The Philosopher's Bacterium

Picture the mediaeval alchemist, standing before a smoking crucible, adding ingredients and performing the requisite incantations. Eventually, he allows the crucible to cool so that he might examine the results. Has he succeeded? Has he achieved his goal of extracting pure gold from the base earth? Alas, he has not*, because he is only human, and he lacks the powers of a Geovibrio.

*For which we should perhaps be grateful. To quote King Midas in an episode of Concrete Cow, "I really should have foreseen the inflationary effect of all that new gold on our economy".

Deferribacter desulfuricans, photographed by K. Takai.

Geovibrio ferrirudecens is a species belonging to the 'phylum' Deferribacteres, an assemblage of Gram-negative bacteria known as yet from only a small number of species. However, the known species are all quite ecologically disparate, so we may have only scratched the surface of deferribacterial diversity. All are anaerobic organotrophs, utilising various organic compounds as electron donors in respiration*. Species vary in their temperature preferences from mesophily (growing at 'room temperature') to moderate thermophily (up to about 60°C). Cells may be immobile rods, or they may be motile with a single polar flagellum (bipolar flagella have been observed in Denitrovibrio acetiphilus, indicating reproduction by budding). Cells of Geovibrio, at least, can occur in chains as well as individually. Known habitats of Deferribacteres include water in oil reservoirs for Deferribacter thermophilus (Garrity & Holt 2001), Japanese hot springs for Calditerrivibrio nitroreducens (Iino et al. 2008), hydrocarbon-contaminated soils for Geovibrio ferrireducens (Garrity & Holt 2001), and the epithelial lining of a mouse intestine for Mucispirillum schaedleri (Robertson et al. 2005). With regard to this last genus, it stands as a good example of how poor is our understanding of real bacterial diversity that a significant component of the intestinal flora of a major model organism was not identified until 2005! When people express surprise to me that there are still new species of organism to be described in the world, I inform them that, at the microbial level, there are almost certainly undescribed species living on you right now.

*As do we, of course. If you remember your high school biology, you'll recall that human respiration reacts glucose and oxygen to produce carbon dioxide and water. In this reaction, glucose is the electron donor while oxygen is the electron receptor.

Geovibrio ferrireducens with periplasmic gold deposits, from Kashefi et al. (2001).

Species of Deferribacteres also vary in their preferred electron receptors. Calditerrivibrio nitroreducens, as indicated by its species name, reduces nitrate, converting it into ammonium. The very recently described Seleniivibrio woodruffii utilises selenium and arsenic compounds (Rauschenbach et al. 2013; arsenate-respiring bacteria can be significant to public health as they convert arsenates to more soluble arsenites, causing arsenic to leach into groundwater). Deferribacter thermophilus and Geovibrio ferrireducens each received part of their names because they grow off ferric iron (Fe³⁺), converting it into ferrous iron (Fe²⁺). Ferrous iron is much more soluble than ferric iron, so iron-reducing bacteria can cause corrosion to iron structures. Both these taxa may also use other electron acceptors. Deferribacter can grow off manganese(IV) or nitrate. Geovibrio doesn't reduce either of those substances, but it has been shown that it can use hydrogen as an electron donor to reduce soluble gold(III) to elemental gold, which becomes deposited in the periplasmic space between the cell membranes (Kashefi et al. 2001). Geovibrio is only one of a number of bacteria that can pull off this trick, and it has been bacteria may have been responsible for the creation of many of the world's gold deposits. When the alchemist of our opening paragraph was struggling with his proto-chemistry, he should have been examining his biology.

REFERENCES

Garrity, G. M., & J. G. Holt. 2001. Phylum BIX. Deferribacteres phy. nov. In Bergey’s Manual of Systematic Bacteriology, 2nd ed., vol. 1. The Archaea and the Deeply Branching and Phototrophic Bacteria (Boone, D. R., R. W. Castenholz & G. M. Garrity, eds) pp. 465-471. Springer.

Iino, T., T. Nakagawa, K. Mori, S. Harayama & K. Suzuki. 2008. Calditerrivibrio nitroreducens gen. nov., sp. nov., a thermophilic, nitrate-reducing bacterium isolated from a terrestrial hot spring in Japan. International Journal of Systematic and Evolutionary Microbiology 58: 1675-1679.

Kashefi, K., J. M. Tor, K. P. Nevin & D. R. Lovley. 2001. Reductive precipitation of gold by dissimilatory Fe(III)-reducing Bacteria and Archaea. Applied and Environmental Microbiology 67 (7): 3275-2279.

Rauschenbach, I., V. Posternak, P. Cantarella, J. McConnell, V. Starovoytov & M. M. Häggblom (in press, 2013) Seleniivibrio woodruffii gen. nov., sp. nov., a selenate- and arsenate-respiring bacterium in the Deferribacteraceae. International Journal of Systematic and Evolutionary Microbiology.

Robertson, B. R., J. L. O’Rourke, B. A. Neilan, P. Vandamme, S. L. W. On, J. G. Fox & Adrian Lee. 2005. Mucispirillum schaedleri gen. nov., sp. nov., a spiral-shaped bacterium colonizing the mucus layer of the gastrointestinal tract of laboratory rodents. International Journal of Systematic and Evolutionary Microbiology 55: 1199-1204.

The Rhodospirillales: It's Photosynthesis, But Not As You Know It

Colony of Rhodospirillum rubrum, from here.
For today's post, I'm going to take a look at the Rhodospirillales. This is a clade within the larger bacterial group known as the Alphaproteobacteria, other members of which include the disease-causing rickettsiae (thought to be close relatives of the ancestors of eukaryote mitochondria) and the nitrogen-fixing bacteria found in legume nodules. Rhodospirillales species are commonly found in fresh water, though some significant species have been found in other habitats. Many (but far from all) species of Rhodospirillales contain a chlorophyll-like pigment called bacteriochlorophyll a that functions like chlorophyll in catalysing photosynthesis. They also often contain other photosynthetic pigments, carotenoids, that are red in colour: hence the common use of prefixes such as 'rhodo-' and 'roseo-' in genus names in this group. Most photosynthetic Rhodospirillales differ from plants in being photoheterotrophs rather than photoautotrophs: that is, they cannot use carbon dioxide alone as the source of carbon in photosynthesis, and require other carbon sources (Rhodospirillum can grow photoautotrophically if conditions are optimal). Rather than using water as an electron donor, photosynthetic Rhodospirillales generally use other donors such as sulfide or hydrogen.

Individual of Magnetospirillum magneticum, showing the row of magnetosomes, photographed by Richard B. Frankel.
The members of the Rhodospirillales are divided between two families, the Rhodospirillaceae and Acetobacteraceae (Garrity et al. 2005). The majority of members of the Rhodospirillaceae are spiral in shape and grow in anoxic or microaerobic conditions. Acetobacteraceae, in contrast, are most often coccus- or rod-shaped and aerobic. Non-photosynthetic members of Rhodospirillaceae include the nitrogen-fixing genus Azospirillum, often found living in the soil or in association with plants (though, unlike the more familiar nitrogen-fixing genus Rhizobium, Azospirillum is not found specifically in association with root nodules). Also noteworthy is the genus Magnetospirillum, specimens of which possess a row of magnetite-containing bodies called magnetosomes down one side of the cell. These magnetic bodies are presumed to aid the bacterium in navigation relative to the earth's magnetic field. Magnetospirillum can be drawn from sediment through the use of a bar magnet; when observed under a microscope close to a magnet, they can be seen to swim parallel to the magnetic field lines. A cell suspension dropped onto a magnetic stirrer will be seen to flicker, as the cells change their direction of movement (and hence the direction of light scattering) to follow the spinning field.

Dividing cell of Stella vacuolata, from Garrity et al. (2005). Scale bar equals 1 µm.
Non-photosynthetic members of the Acetobacteraceae include the acetic acid bacteria (hence the name of the family). These gain energy by converting ethanol to acetic acid or, in more general terms, alcohol to vinegar. Some genera, such as Acetobacter and Acidomonas, are able to further oxidise the acetate produced to water and carbon dioxide; others, such as Gluconobacter, do not do so. One particularly distinctive genus in the Acetobacteraceae is Stella, species of which are found in soil and animal faecal matter. Cells of Stella are flat and, as suggested by their name, star-shaped with six points. Division of Stella involves the growth of a cross-wall down the midline of the cell, with each daughter cell retaining three of the parent's points to which they add three new points.

REFERENCES

Garrity, G. M., D. J. Brenner, N. R. Krieg & J. T. Staley. 2005. Bergey's Manual of Systematic Bacteriology, 2nd ed., vol. 2. The Proteobacteria, part C. The Alpha-, Beta-, Delta-, and Epsilonproteobacteria. Springer.

The Nostocaceae: Tangled Filaments

Macroscopic growth of the cyanobacterium Nostoc commune, from here.

The cyanobacteria, commonly referred to as the 'blue-green algae', were one of the first groups of bacteria to be recognised as distinct. As our knowledge of bacteria has improved over the years, the distinctiveness of cyanobacteria continues to be supported: they are the only bacteria to contain chlorophyll, capturing energy from the light through the oxidation of water. Unfortunately, this confidence in their separation has not necessarily been carried over at lower levels. Many cyanobacterial 'families' and 'genera' have not been supported by more recent molecular analyses. Nevertheless, one clade that has been well supported is the nitrogen-fixing cyanobacteria, Hormogoneae.

Morphology-based classifications of cyanobacteria started, firstly, with the question of whether a species existed as independent cells, or whether they formed thread-like chains. The Hormogoneae are all chain-forming species, with the chain contained within a but they are also distinguished by the formation of heterocysts, large morphologically distinct cells within the chain that specialise in nitrogen fixation. Heterocysts are so specialised that they are unable to photosynthesise for themselves and are dependent on their neighbour cells for nutrition. So, with the presence of differentiated, interdependent cells, Hormogoneae can be regarded not simply as colonies of cells but as true, multicellular bacteria. A number of species of Hormogoneae (particularly in the genus Nostoc) form symbiotic associations with plants that take advantage of their nitrogen-fixing properties. One of the best-known examples is the association of the aquatic floating fern Azolla with the cyanobacterium 'Anabaena' azollae, and Azolla is used as a source of nitrogen in rice paddies. In another post, I have described the association between a Nostoc species and the plant genus Gunnera.

Trichomes of Anabaena, from here. The yellowish cells are heterocysts.

Within the Hormogoneae, classifications have traditionally distinguished between the orders Nostocales and Stigonematales. Stigonematales have branching trichomes, while those of Nostocales are unbranched. The Nostocales have been divided between the Nostocaceae, Rivulariaceae and Scytonemataceae: Rivulariaceae have trichomes that show a distinct base-to-apex polarity, while those of Scytonemataceae show a feature called 'false branching'*. Nostocaceae are defined by the lack of these features: however, it should not be surprising that molecular studies have not supported a group defined solely by the absence of characters, and both Rivulariaceae and Scytonemataceae (and possibly Stigonematales as well) are probably derived (possibly polyphyletically) from 'nostocacean' ancestors. However, actual relationships within the Hormogoneae remain poorly resolved, and no formal reclassification has been proposed (one of the authoritative texts on bacterial classification, Bergey's Manual of Systematic Bacteriology, replaces the cyanobacterial 'orders' with numbered subsections [Nostocales, for instance, is treated as Cyanobacteria subsection IV]—Castenholz 2001).

*True branching as in Stigonematales occurs when cells within a trichome divide at right angles to the direction of the trichome. In 'false branching', the trichome breaks within the containing sheath and then grows out of the sheath, but the division of the individual cells remains linear.

Trichomes of Cylindrospermum licheniforme, from André Advocat. The heterocysts are the round terminal cells, while the large elongate cells behind them are akinetes.

Phylogenetic analyses have also failed to confirm many of the genera recognised within the Nostocaceae (treated by Bergey's Manual as 'form-genera' only), distinguished by features such as whether trichomes are generally straight or coiled, and the positions within the trichome of heterocysts and other specialised cells called akinetes, thick-walled cells that function as resistent spores. The traditional genus Nostoc also differs from other Nostocaceae by the formation of hormogonia, motile trichomes with smaller cells and without differentiated heterocysts. Hormogonia form the dispersal stage of the Nostoc life cycle; it is as hormogonia, for instance, that symbiotic Nostoc are transmitted to new hosts. Mature Nostoc trichomes are embedded in a gelatinous matrix, and in some species this matrix may form a globular ball containing large numbers of radially arranged trichomes. Though usually microscopic, these globular clusters can get very large, sometimes more than twenty centimetres in diameter. Species attributed to other genera of Nostocaceae do not generally produce differentiated hormogonia (though some do, such as the aforementioned Anabaena azollae). Trichomes of these species may remain motile throughout the life cycle, or they may be permanently immotile (the latter state is characteristic of planktonic species).

REFERENCE

Castenholz, R. W. 2001. Phylum BX. Cyanobacteria. Oxygenic photosynthetic bacteria. In: Boone, D. R., & R. W. Castenholz (eds) Bergey's Manual of Systematic Bacteriology 2nd ed., vol. 1, pp. 473-599. Springer.

The Attack of Mega-matrix

Lienau, E. K., R. DeSalle, M. Allard, E. W. Brown, D. Swofford, J. A. Rosenfeld, I. N. Sarkar & P. J. Planet. 2010. The mega-matrix tree of life: using genome-scale horizontal gene transfer and sequence evolution data as information about the vertical history of life. Cladistics 26: 1-11.

The last two decades have seen a great deal of discussion about the role of horizontal gene transfer (HGT) in phylogenetic reconstruction of prokaryotes. That HGT occurs among prokaryotes, occassionally between members of far distant lineage, is undeniable; the question is whether HGT is a common event in bacterial evolution or whether it is mere occasional noise. Some researchers have gone so far as to argue that HGT is so rampant among prokaryotes that the reconstruction of a reliable tree of life for bacteria is an impossibility. As I've noted elsewhere, I have to admit to a certain degree of hostility towards this idea, but I immediately have to confess that this hostility is entirely due to personal prejudice (I really want there to be a tree of life for prokaryotes) and not supported by anything rational.

Attempts to reconstruct the prokaryote tree of life have usually attempted to circumvent the issue of HGT by focusing on a small subset of genes that are believed to be resistant to this problem, such as ribosomal RNA genes. However, this method carries two major issues: (1) the assumption that horizontal transfer of these genes is not possible may not be as robust as believed (some have suggested that there may be no such thing as a truly HGT-free gene), and (2) the smaller the data set used, the greater the chance that other complicating factors may interfere with results. For instance, it is now generally accepted that high-level phylogenetic reconstructions of eukaryotes using rRNA are very vulnerable to the effects of inequal evolutionary rates, with many supposedly 'basal' branches being shown to in fact be highly derived. There is no a priori reason to assume that the same problem would not apply to rRNA phylogenies of prokaryotes.

A paper just published in Cladistics takes the opposite approach to the problem: it uses an absolutely enormous amount of data to see whether a coherent tree can still be recovered. Two main data sets were used analysing 166 genomes from taxa throughout the tree of life (mostly prokaryotes). One concatenated direct amino acid sequences from 12,381 genes to provide 846,999 phylogeny-informative characters (out of a potential 4,540,579 characters). The other compared presence vs absence of genes from the 166 genomes. Analysis was done using parsimony, which is potentially problematic for sequence data but probably necessary to simply work with this amount of data. One analysis was run on the sequence data alone; another was run using the combined sequence and gene presence/absence data (the gene presence/absence data alone had been analysed by an earlier study).



The heartening result of this analysis is that a coherent phylogeny was recovered, particularly using the combined data set (shown above from the paper; a few anomalies were present using the sequence data alone). Most previously recognised major bacterial groups analysed were recovered by the combined data as monophyletic* (the only exception being the spirochaetes, with Leptospira failing to associate with the two Spirochaetaceae). Many of the higher-level relationships were also congruent with earlier proposals: α-proteobacteria as sister to the clade of β- and γ-proteobacteria, with δ-proteobacteria the next group out; a clade of the sphingolipid-producing bacteria (Chlorobium + Bacteroidales; and a clade uniting ε-proteobacteria with Aquifex + Thermotoga, which would then include all known hydrogen-oxidising Eubacteria. It appears unlikely that HGT fatally compromises large-scale analyses.

*Or perhaps I should say 'congruent'. As far as I can see, the study glosses over the question of the rooting of the tree of life; the tree shown is rooted between Neomura (Archaea + eukaryotes) and Eubacteria but no discussion is given on that position.

Of course, the tree is not without warning signs. The aforementioned polyphyletic spirochaetes are a bit worrying in light of the distinctive spirochaete ultrastructure. Some of the relationships within the major clades are a bit off: Gloeobacter is nested well within other cyanobacteria rather than being the most divergent (Gloeobacter is the only known cyanobacterium to lack thylakoids), and the arrangement of eukaryotes is all wrong. However, it must be stressed that, as large as this study was, the taxa analysed still represent only a small proportion of the world's total diversity. What is more, the choice of organisms to have their whole genome sequenced (a necessary pre-requisite for this study) has not been evenly distributed through prokaryote diversity. Many little-studied but potentially phylogenetically significant taxa (such as many of the low-diversity bacterial 'divisions') are significant by their absence, as are many significant subgroups of those divisions that are represented. This story is not yet over.

Bacteria, Too, Grow Old and Die

Stalked Caulobacter crescentis cell giving rise to a flagellate swarmer cell. Photo from here.

Commentors on a recent post here began arguing the side issue of bacterial immortality (derived from the question of whether the last universal common ancestor of all living organisms is extinct or whether it, in some way, is still with us today). Though the argument, as presented in the comments, was largely semantic, the central point was summed up by Don Cox in the statement: "When a cell divides (or multiplies) into two identical cells, you cannot say that one or other is an offshoot". This is a common textbook representation of binary fission as practiced by most bacteria and many eukaryotes*. As with many textbook representations, it is highly likely to be wrong.

*Or most, depending (again) on your choice of semantics. After all, you yourself multiply by binary fission, at least at the internal level.

Any cell, whether bacterial, eukaryote or what have you, is constantly bombarded throughout its life by inimical factors. Toxic substances build up, whether ingested from the outside world or produced as by-products of the cell's own metabolism. DNA and other vital cellular structures become damaged or otherwise functionally altered (for instance, by the process of DNA methylation). As this damage builds up, the cell 'ages' and, if the damage becomes too great, dies. One of the reasons cells multiply in the first place is to counter-act the build-up of these inimical factors. For instance, replication of a chromosome will produce a daughter chromosome in which the damage to the original has been repaired (I'm over-simplifying matters, of course, but you get the idea).

To return to Don's statement above, the crux of the error lies in the belief that the "cell divides... into two identical cells" (emphasis added). But the two resulting cells of binary fission are not necessarily identical if the distribution of the original parent cell's accumulated inimical factors is not even. It may be possible that one cell receives the bulk of the problems while the other cell is left 'clean' (Nyström, 2007). Such uneven division has long been recognised in unicellular organisms such as bakers' yeast Saccharomyces cerevisiae that reproduce by budding, which after all is essentially fission in which the distribution of cytoplasm between the resulting cells is uneven. The budded 'daughter' cell contains little inimical factors when produced while the 'parent' cell retains the bulk. The first record of aging in a bacterium was also in a budding species, Caulobacter crescentis. In Caulobacter, a sessile stalked cell gives rise to a mobile swarmer cell (which will itself eventually develop into a stalked cell). However, each time the stalked cell produces a swarmer cell, it takes longer to produce the next one. It becomes old.


Figure from Stewart et al. (2005) showing the fates of Escherichia coli cell ends over successive generations.

Demonstration of similar aging in Escherichia coli, which produces superficially identical cells through fission, was achieved by Stewart et al. (2005). Rod-shaped E. coli cells multiply by elongating then dividing transversely across the middle so each daughter cell ends up with one of the original cell ends plus one newly produced end. But if we follow the cells to the next generation then one of their daughter cells will have an end that has persisted across at least two divisions while the other will have persisted for only one. One cell is therefore 'older' than the other and Stewart et al. discovered that 'older' cells took longer to grow and reach division than 'younger' cells. Based on the rate at which reproduction of older cells slowed down over successive generations, Stewart et al. calculated that a given cell end would persist for about 100 generations which also matches the rate of aging calculated for Caulobacter stalked cells. Similar aging has also been demonstrated in the fission yeast Schizosaccharomyces pombe, a eukaryote that multiplies by equal binary fission.

As summarised by Nyström (2007), evolutionary modelling has indicated that asymmetric division of aging factors during multiplication may offer a selective advantage. Essentially, the chamces of one rejuvenated cell surviving and reproducing, even at the expense of producing one elderly cell, may outweigh those of two mediocre cells. Whether the aging process demonstrated by Stewart et al. (2005) leads to eventual cell death in nature remains unconfirmed but it does seem a very likely inference.

REFERENCES

Nyström, T. 2007. A bacterial kind of aging. PLoS Genetics 3 (12): e224. DOI: 10.1371/journal.pgen.0030224.

Stewart, E. J., R. Madden, G. Paul & F. Taddei. 2005. Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biology 3 (2): e45. doi:10.1371/journal.pbio.0030045

The Endosymbiotic Hammer Strikes Again

I was going to write a post here about Lake's (2009) proposal in yesterday's Nature that double-membraned (Gram-negative) bacteria could be derived from an endosymbiotic relationship between two single-membraned bacteria (see this earlier post for an explanation of double- versus single-membraned bacteria), and why I found it decidedly unconvincing. But I've spent today trying (unsuccessfully, I might add) to look at seminal receptacles in harvestman ovipositors and overexposure to the smell of clove oil has left me feeling decidedly crook and put my brain into shutdown. So I'll just give you the link and the abstract, and a few things to keep in mind when reading the article (if you can get access to it):

Lake, J. A. 2009. Evidence for an early prokaryotic endosymbiosis. Nature 460: 967-971.

Endosymbioses have dramatically altered eukaryotic life, but are thought to have negligibly affected prokaryotic evolution. Here, by analysing the flows of protein families, I present evidence that the double-membrane, Gram-negative prokaryotes were formed as the result of a symbiosis between an ancient actinobacterium and an ancient clostridium. The resulting taxon has been extraordinarily successful, and has profoundly altered the evolution of life by providing endosymbionts necessary for the emergence of eukaryotes and by generating Earth’s oxygen atmosphere. Their double-membrane architecture and the observed genome flows into them suggest a common evolutionary mechanism for their origin: an endosymbiosis between a clostridium and actinobacterium.

Point 1: If such an endosymbiosis had occurred, then both partners would have probably had cell walls (peptidoglycan layers) outside their membrane (the only single-membraned eubacteria lacking cell walls are Mollicutes, which are parasites of eukaryotes*). Why did the external partner lose its cell wall rather than the internal partner?

*I originally referred to Mollicutes as intracellular - thankfully, Elio Schaechter put me right (they're extracellular). I did say that my brain had stopped working.

Point 2: The endosymbiosis scenario requires that the genetic complement of the external partner be entirely lost or transferred to the inner partner (as well as the greater part of its cytoplasm). While unusual, this would not be unique. Transfer of genes from one partner to the other is a common (if not universal) event in endosymbioses. The hydrogenosomes found in some anaerobic eukaryotes are generally accepted to be derived from mitochondria, but most have entirely lost their genomes (as far as we know). Also, in most secondary or tertiary chloroplasts, the eukaryotic genome of the endosymbiont has disappeared. However:

Point 3: In all established cases of endosymbiosis, gene transfer or loss has been mostly (if not entirely) to the cost of the internal partner. This applies not just to mutualist endosymbionts, but also to intracellular parasites. Lake's proposed endosymbiosis requires the transfer to happen the other way, at the cost of the external partner (offhand, the same objection applies to scenarios that propose an endosymbiotic origin for the eukaryotic nucleus).

Point 4: Even if Lake's premise that double-membraned bacteria carry genes from two phylogenetically separate ancestors is correct (I have to confess that I don't feel knowledgeable enough to critique that point), that doesn't necessarily require an endosymbiosis. A simple symbiosis might possibly be sufficient. Many bacteria form closely-linked ectosymbiotic consortia, and the well-established propensity of bacteria to swap genetic material like trading cards could result in a substantial transfer in such an arrangement over time. Also:

Point 5: Among eukaryotes, the endosymbiosis theory receives something of a boost from the point that eukaryotes are absolutely lousy with endosymbionts at all stages of interdependence. Lake mentions the proteobacterium Buchnera in aphids; there are also zooxanthellae in corals and clams, Perkensiella in amoebae, a whole universe of intracellular parasites... the list goes on. Prokaryotes, in contrast, just don't seem to carry endosymbionts to the same degree. Lake mentions in his support that the aforementioned Buchnera carries its own endosymbiont; what he doesn't mention is that this is the only well-established case of an endosymbiont inside a prokaryote. Lake claims that the Chlorochromatium consortium is very close to an endosymbiotic relationship. It's still ectosymbiotic nonetheless. Contrast this with the extreme general diversity and versatility of prokaryotes, which is leagues ahead of that of eukaryotes - you'd think that if they could easily do it, they would be.

Point 6: The presence of a nucleus of sorts in Planctomycetaceae indicates that bacteria are not incapable of developing new membrane systems.

Point 7: I really, really hate this paragraph:

In fact, the membrane organization of double-membrane prokaryotes fundamentally differs from that found in single-membrane prokaryotes. In the former, the peptidoglycan layer is sandwiched between the outer and inner membranes, so that it surrounds the inner membrane: in contrast, in the latter there is no inner membrane, and the peptidoglycan layer, located outside the cell, surrounds the outer membrane. Also, double-membrane prokaryotes contain their flagellar motors in the inner membrane, whereas single-membrane prokaryotes contain their flagellar motors in the outer membrane. And the photosynthetic apparatus in double-membrane prokaryotes is in the inner membrane, rather than in the outer membranes as in single-membrane prokaryotes. In other words, the organization of the inner membrane of the double-membrane prokaryotes resembles that of the outer membranes of typical single-membrane prokaryotes. The inner membranes of double-membrane prokaryotes are organized almost as if they were derived from the outer membrane of an engulfed single-membrane prokaryote.

This, ladies and gentlemen, is a classic case of semantic silly buggers. Lake obfuscates the difference between single- and double-membrane bacteria by noting that double-membrane bacteria have an outer and inner membrane, then referring to the membrane in single-membrane bacteria as the outer membrane even though it is positionally comparable to the inner membrane (pause to wipe foam from frothing mouth and allow bulging eyeballs to return to their sockets). His referral to the supposed difference between flagella of the two types of bacteria looks a little different when you consider that what he is saying is that both anchor their flagella on the membrane inside the cell wall. (noooo! the family curse!)

Point 8:

There is currently much discussion of the prokaryotic ‘tree of life’, but there are few points of agreement regarding its topology, except that it is not a tree.

While the idea that a tree is not an appropriate expression of prokaryote evolution is increasingly popular, I think it's jumping the gun a little to present it as a consensus. Take a look at the number of trees in an average issue of the International Journal of Systematic and Evolutionary Microbiology, for a start (and yes, now I am just picking at minor details).

Point 9: And just on a final quibble, this line from the supplementary info:

I propose the name Domain Synergia (Gr. Synergia – joint work) for those prokaryotes that possess the Gram negative, double membrane organization, and are derived from large, statistically significant gene flows from both the Actinobacteria (as defined in Table S1) and the Clostridia (also as defined in Table S1).

Not only would I consider it fairly unacceptable to bury the publication of a new taxon name within the online-only supplementary info of a print-based article, but under Lake's proposed scenario this "new" taxon would be circumscriptionally equivalent to the already-available name of Didermata.

Pathogens, or More than Pathogens? (Taxon of the Week: Aeromonas)

Dropsy in a goldfish infected with Aeromonas hydrophila. Keepers of freshwater fish will probably be all too sadly familiar with this sight - dropsy is highly contagious, and almost impossible to eliminate once it becomes established (of course, fish not being great exhibitors of external symptoms, "once it becomes established" is roughly equivalent to "by the time you notice that something's happening"). Image from MicrobeWiki.

Yeah, it's late. Tough. What with moving house over the weekend, having learnt that I had to move on Monday (long story), I've been a little preoccupied. I rather doubt that anyone marks their calendar for these posts anywho.

Anyway, Aeromonas is a genus of rod-shaped facultatively anaerobic gamma proteobacteria that is abundant in aquatic habitats (mostly freshwater). 16S rDNA phylogenetically speaking, it belongs to a clade that also includes the Vibrionaceae, Pasteurellaceae and Enterobacteriaceae, all of them pretty economically significant families because they all contain common pathogens, and Aeromonas follows suit. Of the about fifteen species currently recognised in the genus, at least five have been implicated in human infections, while the others are known primarily as pathogens of aquatic organisms such as fish and frogs. The most common symptoms of Aeromonas infection are gastrointestinal diseases (just to make you wince, a quote from Janda & Abbott, 1998 - "Chronic diarrhea exceeding 1 year's duration due to [Aeromonas] caviae or A. hydrophila has been recorded"), but conditions such as septicaemia, wound infections or even meningitis have been caused by this genus, among others.


Human leg infected with Aeromonas hydrophila. Photo from Microbe Wiki.

So far, Aeromonas species have been almost entirely studied as pathogenic and/or animal-associated organisms. However, they have been isolated in large numbers from freshwater and brackish habitats (particularly nutrient-rich ones) (Kaper et al., 1981; Martin-Carnahan & Joseph, 2005), and, in comparison with other genera such as Streptococcus, Staphylococcus and Vibrio, appears to me to show every sign of being primarily a facultative pathogen. Infection causes a range of pathologies, with no obvious standard symptom arc*, low host specificity, and without a tight correlation between the presence of Aeromonas and whether or not a pathology develops (Aeromonas has been isolated from the gut of patients with no sign of Aeromonas-related pathologies). Compare this to an obligate pathogen such as Treponema pallidum (the cause of syphilis), which causes a more standardised range of symptoms and for which presence of the pathogen almost always leads to presence of the disease**. It is quite possible that Aeromonas' role in the environment as a pathogen is in fact only secondary to whatever else it's doing out there (my first guess would be decomposition). However, this neglect of Aeromonas' environmental ecology is hardly unusual. The truth is that our knowledge of environmental real-time ecology for all bacteria is depressingly low. Not only have pathogens received the greater share of attention, but even studies of non-pathogenic taxa have generally been conducted in highly artificial laboratory environments (for obvious reasons of practicality). Laboratory culture media, for instance, generally offer a uniform abundance of nutrients that is entirely unlike the poorer and more patchy nutrient distributions elsewhere, and it is a very open (and very difficult) question how much and in what way observations made in the laboratory environment really reflect what happens elsewhere.

*Yeah, you can tell I'm not thoroughly briefed in my medical terminology and I'm just making this up as I go along, can't you?

**Anybody out there with actual medical knowledge can feel free to rip into me if I've just made an idiot of myself.

Back to Aeromonas. While (as I said) about fifteen or so species are currently recognised, traditionally these have been divided into two groups - Aeromonas salmonicida (guess what it is known to do) vs. everything else. Aeromonas salmonicida is psychrophilic (it grows best at low temperatures, from 2 to 30°C) and nonmotile, while the other species (the 'Aeromonas hydrophila' group) are mesophilic (growing at temperatures between 10 and 42°C) and motile, usually with a single polar (at one end) flagellum but occasionally with lateral flagella. 16S rDNA phylogeny, however, shows that A. salmonicida is nested deep within the genus, and represents a derived taxon. Reflecting this position, A. salmonicida still possesses the genes for flagella production despite their inactivity. And just to really hammer the point home, an as-yet unnamed Aeromonas strain has been isolated (Martin-Carnahan & Joseph, 2005) that is mesophilic, motile, but genetically identical to A. salmonicida!

REFERENCES

Janda, J. M., & S. L. Abbott. 1998. Evolving concepts regarding the genus Aeromonas: an expanding panorama of species, disease presentations, and unanswered questions. Clinical Infectious Diseases 27: 332-344.

Kaper, J. B., H. Lockman, R. R. Colwell & S. W. Joseph. 1981. Aeromonas hydrophila: ecology and toxigenicity of isolates from an estuary. Journal of Applied Microbiology 50 (2): 359-377.

Martin-Carnahan, A., & S. W. Joseph. 2005. Genus I. Aeromonas Stanier 1943, 213^AL. In G. M. Garrity, D. J. Brenner, N. R. Krieg & J. T. Staley (eds) Bergey's Manual of Systematic Bacteriology, 2nd ed., vol. 2. The Proteobacteria. Part B. The Gammaproteobacteria, pp. 557-578. Springer.

Most Unbelievable Organisms Evah!

Last week I asked for nominations for the title of Most Incredible Organism Ever. Thank you very much to those of you who responded with your selections. Some of them were organisms I'd already selected myself, some of you reminded me of amazing organisms that were even better than the ones that I'd considered*. Certainly, getting the list down to ten top nominations was not easy, and I'm sure anyone else would have chosen differently from myself. Allen Hazen pointed out that, strictly speaking, "incredible" means "inspires disbelief", and certainly some of the things I have lined up do exactly that.

*As an aside, something that never fails to amuse is looking up what Google search terms have brought people to Catalogue of Organisms. Trust me, "amazing organism" is bound to bring in the punters.

Honorable mentions should be given to those organisms that people nominated that I didn't end up using, because they're certainly all incredible. Allen Hazen suggested the platypus, while Alan nominated the aye-aye. Dave Coulter was all for the Osage orange, while Amie Roman asked me to "pick an onychophoran, any onychophoran".

But I'm afraid I ended up passing over these wonders. In no particular order, here are my nominations for "Most Incredible Organism" (click on the pictures to be taken to their source):



Homo sapiens Linnaeus, 1758: Both myself and Mike Keesey agreed on this one. As much as I hate to stoke this species' notoriously smug satisfaction, it has to be admitted that humans are pretty amazing. Douglas Adams once explained that "The History of every major Galactic Civilization tends to pass through three distinct and recognizable phases, those of Survival, Inquiry and Sophistication, otherwise known as the How, Why and Where phases. For instance, the first phase is characterized by the question How can we eat? the second by the question Why do we eat? and the third by the question Where shall we have lunch?" As far as we know, Homo sapiens is the only species on this planet to have reached Adam's second stage, let alone the third.



Polyascus polygenea (Lützen and Takahashi, 1997): Polyascus polygenea is a member of the Rhizocephala, notorious crustacean parasites of crabs. The larval rhizocephalan looks very similar to the larva of a barnacle (to which it is closely related), but when it finds a decapod host it burrows in and transforms into an almost fungus-like mass spreading through the hosts body. The only externally visible part of the parasite is its large egg-sac (the orange tube in the picture above, which does not show a Polyascus but another rhizocephalan species, Peltogaster paguri). The rhizocephalan egg-sac grows at the base of the crab's tail, where it would normally hold its own eggs. In order to make sure this spot is free, the rhizocephalan chemically castrates its host, preventing it from ever reproducing. It also affects its host's behaviour so that the crab lovingly tends the parasite's egg-sac as if it were its own. So powerful is the parasite's mental ju-ju that even male hosts that would not naturally produce eggs will tend the parasite just as a female would.

Vasha nominated the best-known rhizocephalan, Sacculina carcini, but I've decided to go with Polyascus polygenea because this species adds a further twist to the tale. A single Sacculina larva will give rise to a single egg-sac. But Polyascus reproduces within the host asexually by budding, so that one larva will give rise to multiple egg-sacs (Glenner et al., 2003).

Polyascus is also acting as the stand-in for all mind-controlling parasites. As we learn more about the natural history of parasitic organisms, it turns out that behavioral control of parasites over their hosts is not uncommon. Parasitic wasps make caterpillars guard the wasp's cocoons. Horsehair worms make crickets drown themselves so the aquatic adult worm can emerge. Tanya reminded me about Cordyceps unilateralis, a fungal parasite of ants that, when it's ready to produce spores, makes its host climb to the highest available point so that the spores will spread as far as possible. The ways of parasites are disturbing. And speaking of disturbing...



Acarophenax tribolii Newstead & Duvall, 1918: It is not uncommon for pregnant women to express delight at feeling their baby kick inside them. But what if it was doing more than just kicking? Mites of the genus Acarophenax are parasites of beetles that can claim to have perhaps the just-plain-ickiest life history of any animal. The sex ratio of this genus is highly skewed - depending on the species, a brood may contain up to thirty females, but usually only a single male. These offspring reach sexual maturity before they are even born, and the male proceeds to fertilise all of his sisters while still within their mother. In fact, the male doesn't even survive to become free-living - by the time the already-fertilised females emerge from their parent, the male has reached the end of his short (but extremely busy) lifespan. The advantage to the mite in this twisted incestuous life cycle? An exceedingly short generation time, of course - Acarophenax mahunkai, for instance, has a generation time of only three to five days (Steinkraus & Cross, 1993).



Mites of the closely related family Pyemotidae have a similar life cycle - the offspring reach full sexual maturity while in their mother, and begin copulating the instant that they emerge from their proud parent. Females of Pyemotes herfsi (shown in the picture above), known as "itch mites" and facultative biters of humans, can produce more than 250 fully mature offspring.



Welwitschia mirabilis Hook.f.: I also have to thank Tanya for reminding me of the wonder that is Welwitschia. Welwitschia mirabilis is unique to the Namib Desert in Angola and Namibia, and is a member of the gymnosperm order Gnetales along with the genera Ephedra and Gnetum. The Gnetales have received a lot of attention due to their much-debated phylogeny (morphological characters suggest they are the living sister group to angiosperms, while molecular analyses place them closer to conifers), but that's not what's so amazing about Welwitschia. It's not even the bright pink, insect-pollinated cones. What makes this plant so incredible is the way it grows. Welwitschia mirabilis only ever produces two adult leaves, followed by the death of the plant's apical meristem (growing tip). The two strap-like leaves, however, continue to grow indefinitely, and can reach lengths of over eight metres (most individuals look like they have more than two leaves, but this is only because of the leaves splitting as the ends get frayed). Welwitschia is very slow-growing, and individual specimens can live to be hundreds, if not thousands of years old.



Argentinosaurus huinculensis Bonaparte & Coria, 1993: There's no other way to say it - sauropods were just stupidly huge. And Argentinosaurus was one of the most ridiculous of all, being the largest well-characterised sauropod (potentially outdone only by such almost-apocryphal taxa as Amphicoelias fragillimus and Bruhathkayosaurus matleyi). With an estimated total length of nearly thirty metres, and potential weight of up to 80 tonnes... well, there's nothing much that can be said in response except "Whoa".

Sauropods are so huge that when a popular blog was set up dedicated to them, the site authors couldn't fit in the entire animal and were forced to dedicate themselves to a single section. I refer, of course, to the famed Sauropod Vertebra Picture Of the Week - SV-POW!. Rumour has it, however, that a second site is in the works devoted to sauropod crania, to be called "Sauropod Heads - Anatomy, Zoology And Morphology".



Rhizanthella slateri (Rupp) M. A. Clem. & P. J. Cribb, 1984: Rhizanthella is a small genus of three orchid species unique to Australia. What makes Rhizanthella so amazing is that its entire life cycle is spent underground. The plant is saprophytic, dependent on an associated fungus for nutrition, and its stems are entirely subterrean. Even the flowers do not have to break the surface - they are pollinated by minute gnats that can reach them through tiny cracks in the covering litter. The first known Rhizanthella specimens were discovered in 1928 when they were brought up by a farmer's plough, and only intermittent finds were made for a long time afterwards. Even today, their obscure habits mean that Rhizanthella species are poorly known. Sad to say, they are also all regarded as endangered. They are only known from restricted, scattered ranges, limited by the presence of their associated fungus and the tree of which it is in turn connected to mycorrhizally (in Rhizanthella gardneri, the tree is Melaleuca uncinata, but the associations of Rhizanthella slateri are still unknown).

Vasha reminded me of Rhizanthella by telling me of the American saprophytic plant Thismia americana, which also spends most of its life underground with only the minute flowers emerging above the surface. Thismia americana has not been recorded since 1916, and is feared to be extinct, though it is hard to know for certain. As described at the link, an intensive search in the early 1990s failed to find any specimens, but a concurrent dummy run using scattered white beads about the same size as T. americana flowers was also a failure.



Puccinia monoica Arthur, 1912: The object of the photo above is not a flower. It grew from a flowering plant, but it's not a flower. Puccinia monoica is a fungus parasitic on Brassicaceae (mustard) species. Like rhizocephalans on their crabs, Puccinia monoica changes the reproductive biology of its host, preventing it from growing its own flowers. Instead, it makes the host plant grow a tight whorl of leaves, which are covered by the bright yellow sporangia of the fungus. Not only does the fungus-induced 'false flower' look like a real flower, it even produces nectar and scent like a real flower, attracting insect pollinators just like a real flower would (Raguso & Roy, 1998). And just like pollen from a real flower, these pollinators carry spores from fungus to fungus, cross-fertilising the fungi as they do so.



Deinococcus radiodurans (ex Raj et al. 1960) Brooks and Murray 1981: A dose of radiation of 10 joules per kilogram will kill a human being. Sixty joules per kilogram will kill Escherichia coli. Deinococcus radiodurans may look like a fairly unremarkable bacterium at first glance, but it can withstand a radiactive dose of 5000 joules per kilogram and not even blink (that is, if it had eyes they wouldn't blink). It can withstand radiation so strong that its genome is simply blasted to pieces, stoically knitting the fragments back together again afterwards. Deinococcus can withstand extreme heat, extreme cold, and strong acidity. In a pun so bad that it demands to be repeated, this organism has been dubbed Conan the Bacterium. Pavlov et al. (2006) went so far as to suggest that Deinococcus' incredible resilience to radiation indicated an extraterrestrial origin, carried from Mars on an asteroid, but it seems more likely to be a by-product of resilience to other stressors such as desiccation (Cox & Battista, 2005). Still, one can't help wondering if, even if it didn't come from Mars in the first place, it has managed to make it over there on one of Earth's probes.

So resistant is Deinococcus to everything possibly imaginable, in fact, that we still have no idea where it lives naturally. It was first isolated from cans of irradiated beef, and has not yet been found to be abundant in any particular environment. Phylogenetically, Deinococcus forms a clade with the thermophilic bacterium Thermus (one species of which, Thermus aquaticus, is of enormous significance to molecular biology as the source of the Taq enzyme used in PCR). This clade is most commonly referred to (rather unimaginatively) as the Deinococcus-Thermus group, but I personally prefer the name given to them by Cavalier-Smith (2002) - Hadobacteria, the bacteria of Hades.



Proteus anguinus anguinus Laurenti, 1768: The white olm, the only truly cave-dwelling tetrapod (the closely related black olm, Proteus anguinus parkelj, is a surface-dweller). [Update: Much to my chagrinn, Nick Sly has reminded me that there are other cave-dwelling salamanders out there.] I've included the olm not only for its own sake, but as a representative of the entire world of troglobitic and stygobitic fauna (troglobitic animals are those that live in actual caves while stygobitic taxa live buried in the ground, usually in aquifers). In this strange, silent world, animals are almost entirely dependent on food particles washing down from the surface, so life underground is slow, and patient. Troglobites can go for incredible amounts of time without eating - Darren Naish informs us of an olm that was supposedly kept at the Faculty of Biotechnology in Ljubljana without food for twelve years! If that is what a large, complex vertebrate is capable of, imagine what is possible for the smaller invertebrates with their lower metabolic requirements.

And last, but certainly not least:



Wasmannia auropunctata (Roger, 1863): Commonly known as the little fire ant or electric ant (the latter name has been promoted in recent years to dissuade confusion with the larger, not closely related fire ants of the genus Solenopsis), Wasmannia auropunctata is regarded as one of the world's worst invasive organisms. It has been linked with decreases in biodiversity in locations to which it has been introduced, and has a painful sting to boot. It also has one of the world's most remarkable reproductive systems (Fournier et al., 2005). Like other ants, Wasmannia has both haploid males and diploid females, with the females divided between reproductive queens and non-reproductive workers. Genetically, though, Wasmannia is a little different from other ants. While males appear to mate with queens the normal way, only workers are produced by male fertilisation. Any new queens that are produced are genetically identical to their mothers. Still, the male lineage doesn't disappear - somehow, the male genes are able to eliminate the female genes from some of the eggs, and the resulting male Wasmannia are genetically identical to their fathers.

Wasmannia is one of very few organisms that exhibit androgenesis - clonally reproducing males. The only other known natural habitual cases are a cypress species, Cupressus dupreziana, and freshwater bivalves in the genus Corbicula, though odd cases of androgenesis have been recorded in laboratory and cultivated organisms (Hedtke et al., 2008). Effectively, the male and female Wasmannia are reproductively isolated from each other - they are separate species.

REFERENCES

Cox, M. M., & J. R. Battista. 2005. Deinococcus radiodurans — the consummate survivor. Nature Reviews: Microbiology 3 (11): 882–892.

Fournier, D., A. Estoup, J. Orivel, J. Foucaud, H. Jourdan, J. Le Breton & L. Keller. 2005. Clonal reproduction by males and females in the little fire ant. Nature 435: 1230-1234.

Glenner, H., J. Lützen & T. Takahashi. 2003. Molecular and morphological evidence for a monophyletic clade of asexually reproducing Rhizocephala: Polyascus, new genus (Cirripedia). Journal of Crustacean Biology 23: 548-557.

Hedtke, S. M., K. Stanger-Hall, R. J. Baker & D. M. Hillis. 2008. All-male asexuality: origin and maintenance of androgenesis in the Asian clam Corbicula. Evolution 62 (5): 1119-1136.

Pavlov, A. K., V. L. Kalinin, A. N. Konstantinov, V. N. Shelegedin & A. A. Pavlov. 2006. Was Earth ever infected by martian biota? Clues from radioresistant bacteria. Astrobiology 6 (6): 911-918.

Raguso, R. A., & B. A. Roy. 1998. 'Floral' scent production by Puccinia rust fungi that mimic flowers. Molecular Ecology 7 (9): 1127-1136.

Steinkraus, D. C, & E. A. Cross. 1993. Description and life history of Acarophenax mahunkai, n. sp. (Acari, Tarsonemina: Acarophenacidae), an egg parasite of the lesser mealworm (Coleoptera: Tenebrionidae). Annals of the Entomological Society of America 86 (3): 239-249.

How to Kill Tropical Fish

A short while ago I was contacted by Ava of The Reef Tank, a site for keepers of tropical marine aquaria, asking if I would contribute something for their in-house blog. I did once keep a tropical (freshwater) aquarium, but sadly the main thing I learnt from the experience was that putting too much fish in the tank early on leads to their rapid demise due to the buildup of toxic nitrogen compounds (eventually, I discovered the attractive yet indestructable White Cloud mountain minnow). So I presented Ava with a piece on the bacteria responsible for maintaining the nitrogen cycle in fish tanks, and you can read it here.

Streps

Just a quick post for Taxon of the Week this time around - blame it on the time of year (I am definitely one of those who move into full "Bah, Humbug!" mode around this time of year, though personally I always associate the word "humbug" more with The Phantom Tollbooth than A Christmas Carol*). And in this time of year with its tradition of kissing under the mistletoe (or so we're told - that tradition never made it to the Antipodes), what could be more appropriate than an introduction to an organism most commonly associated in the public mind with throat infections?

*Remember that Phantom Tollbooth allusion - hopefully, I will be having cause to make further reference to it within the year.

Streptococcus is one of the most familiar bacterial genera. There was a time when the name was used to refer to almost any spherical, Gram-positive bacterium that grew in a chain-shaped colony, but the old Streptococcus calved off a few genera in the mid-1980s, most notably Enterococcus and Lactococcus. One of the most significant features distinguishing Streptococcus from the latter two genera is that Streptococcus secretes a protective capsule of slimy polysaccharides. In pathogenic species, this capsule apparently mimics the host's connective tissue, allowing the bacterium to pass unnoticed by the host's immune system.

The best-known members of the genus include Streptococcus pneumoniae and S. pyogenes. Streptococcus pneumoniae causes (unsurprisingly) pneumonia. Streptococcus pyogenes causes... well, almost anything that you'd care to mention, really. It's most commonly associated with "strep throat", but it can also cause such dreadful conditions as scarlet fever, toxic shock syndrome and ye olde puerperal fever that caused the death of so many new mothers before Oliver Wendell Holmes suggested in 1843 that getting doctors to wash their hands before delivering a baby was perhaps not such a bad idea. The most infamous (though thankfully, one of the rarest) condition caused by S. pyogenes is necrotising fasciitis - the dreaded flesh-eating bacterium. Yes, it does exist. No, it is not just something invented by B-grade horror movies.

Not all members of Streptococcus are pathogens. Streptococcus thermophilus, for instance, is used in the production of yoghurt. Unfortunately, though all too typically for bacteria, the non-pathogenic taxa have generally been ignored in favour of their more attention-seeking cousins.

REFERENCES

Prescott, L. M., J. P. Harley & D. A. Klein. 1996. Microbiology (3rd ed.) Wm. C. Brown Publishers: Dubuque (Iowa).

The Diversity of Slime Moulds

How could you not love an organism that manages to combine both slime and mould? Slime moulds are saprobic organisms (i.e. they gain their nutrients by breaking down dead organic matter) that spend most of their life cycle feeding as separate amoeboid cells or disaggregated plasmodium. However, when conditions become right all the cells or plasmodium near each other will stream together to form a fungus-like fruiting body that releases spores, as shown in the diagram above borrowed from here. Because slime moulds thus resemble protozoa for part of their life cycle but fungi at other times, they were an early protagonist in the destruction of the idea that all organisms could be divided between plants and animals. Slime moulds, it turns out, are mostly not related to plants or animals. As our understanding of organismal phylogeny has progressed, it has become clear that not all slime moulds are even related to other slime moulds. Instead, the term has been used to cover a number of phylogenetically disparate organisms with little in common other than similar life cycles. However, the majority of references to slime moulds out there fail to mention this, focusing on only a small part of "slime mould" diversity, so I thought I'd give a brief overview of the full diversity of organisms with a slime mould-type life cycle.



1 - Myxogastrea: The plasmodial or acellular slime moulds, also known as Myxomycetes. This is the largest group of "slime moulds" - both in terms of number of species and the size reached by some species. While most other groups of slime moulds are fairly microscopic, myxogastreans reach sizes where they can easily be seen with the naked eye, at which point they are usually mistaken for fungi. During the feeding stage of their life cycle, myxogastreans form a plasmodium - a spreading mass that is not divided into individual cells, like threads of jelly or mucus (photo above from here). Recent phylogenetic analyses agree that myxogastreans belong to the Amoebozoa, the clade that includes more familiar amoeboids such as, well Amoeba (Cavalier-Smith et al., 2004). Indeed, the amoeboflagellate genus Hyperamoeba has been shown to represent a polyphyletic assortment of myxogastreans that have dropped the plasmodial habit.



2 - Dictyostelia: While myxogastreans may be the largest group of slime moulds, dictyostelians may be the most famous, because they take the standard coolness of the slime mould life cycle and turn the dial up to eleven. The photo above from here shows the various stages of the life cycle of the most famous dictyostelian, Dictyostelium discoideum. Dictyostelians are cellular slime moulds - while myxogastreans form a plasmodium, dictyostelians spend their nutritive phase as separate individual amoeboids. When the time comes for reproduction, the separate amoeboids swarm together to form a slug-shaped mass that actually moves as one, like something out of a Japanese cartoon. The dictyostelian slug crawls around until it finds a suitable location, at which point it extends outwards to form a sporangium on the end of a long thin stalk. The complexities of Dictyostelium's life cycle have made it a favoured study organism for such topics as kin selection, as researchers attempt to identify what cues incite slug formation, and why some individual amoeboids forming the sporangium stalk are seemingly willing to sacrifice their own reproductive potential in order to promote the reproduction of those cells forming the sporangium.

Phylogenetically, dictyostelians are also amoebozoans, closely related to myxogastreans. However, analyses are currently unable to resolve whether amoebozoan slime moulds share a single origin (forming a clade called Mycetozoa) or whether dictyostelians and myxogastreans independently originated from closely related but separate amoeboid ancestors.



3 - Protostelia: Three small families of slime moulds, the Protosteliidae, Cavosteliidae and Ceratiomyxidae, form a spreading nutritive phase similar to that of the Myxogastrea, and have often been regarded as closely related to the ultrastructurally similar myxogastreans. However, while myxogastreans form a truly acellular plasmodium, different protostelians form a pseudoplasmodium, with cells retaining their individual identity (Protosteliidae and Cavosteliidae), or a plasmodium that breaks up into individual cells before sporangium formation (Ceratiomyxidae). Ceratiomyxidae form small coral-like fruiting bodies - the photo above by Keisotyo shows a Ceratiomyxa species - while Protosteliidae form minute sporangia on slender stalks like dictyostelians. If mycetozoans form a single group, protostelians may represent a morphological connection between the cellular dictyostelians and the acellular myxogastreans. A relationship between protostelians and other mycetozoans was supported by Baldauf (1999), but the group remains little studied. The protostelians themselves are of doubtful monophyly, and some families may be closer to myxogastreans than others.

4 - Buddenbrockia: One parasitic animal was only recently identified as having a slime mould-like life cycle, with disassociated cells in its host aggregating together to give rise to a worm-like reproductive stage. The sordid details were covered in an earlier post.



5 - Acrasea: Acrasids are cellular slime moulds like dictyostelians, and indeed were once united with dictyostelians under the name of Acrasiomycetes. Like dictyostelians, acrasids live as individual amoeboids that aggregate together to form raised sporangia. The photo above from here shows the fruiting bodies of the best-known acrasid, Acrasis. However, acrasids are ultrastructurally distinct from dictyostelians, and are not even amoebozoans - rather, they belong to a protozoan group called Heterolobosea that also includes Naegleria, the organism that causes amoeboid meningitis, and belongs to the Excavata eukaryote superclade. Whether or not it was due to the mistaken assumption that acrasids were closely related to the intensely studied Dictyostelium, or whether it was due to the fact that acrasids seem to be most often found growing on animal poo, studies of acrasids are laughably rare, and only Acrasis rosea appears to have received any recent attention.

6 - Labyrinthulea: The slime nets are members of the Heterokonta, the clade also including brown and golden algae (among others), and have been covered before at this site - twice, in fact.

One protist group, the Phytomyxa or Plasmodiophoromycota, has often been included with the slime moulds due to its formation of a plasmodium for part of its life-cycle. However, phytomyxans, which are parasites of plant roots belonging to the Rhizaria (the eukaryote superclade including foraminiferans and radiolarians), do not seem to have an aggregative phase of the life-cycle comparable to other slime moulds. The best known phytomyxan is Plasmodiophora brassicae, the cause of club root in cabbages and other brassicas.



7 - Myxococcales: Finally comes a group that has never been regarded as slime moulds, but which has a very similar life cycle. The reason why Myxococcales have never been lumped with slime moulds is because they are not eukaryotes of any kind, but bacteria. Myxococcales are saprobic bacteria generally found in soil. They are capable of gliding motility, a form of movement by means other than flagella, though the exact mechanism remains little known. When nutrient supplies run low, some species of Myxococcales are capable of swarming together in a similar manner to cellular slime moulds and releasing dispersive spores. Myxococcales are therefore one of the few groups of bacteria to have developed multicellularity.

REFERENCES

Baldauf, S. L. 1999. A search for the origins of animals and fungi: comparing and combining molecular data. American Naturalist 154 (S4): 178-188.

Cavalier-Smith, T., E. E.-Y. Chao & B. Oates. 2004. Molecular phylogeny of Amoebozoa and the evolutionary significance of the unikont Phalansterium. European Journal of Protistology 40: 21-48.

Hyphae without Nuclei: Filamentous Bacteria

Sporangia of Streptosporangium nondiastaticum. Image from Atlas of Actinomycetes.

Large size can have its advantages. Pound for pound, a large organism is often more energy-efficient than a small one. A larger organism may have an edge in competing for resources. Larger organisms may be less at risk from predation by other organisms. Therefore, it follows that even when life was a single-cell only affair, things would eventually get bigger. However, large size can also have its disadvantages. If we imagine (for the sake of argument) that the original single cells were roughly spherical, then increase in overall volume occurs much faster than overall surface area - exponentially faster, in fact. As the ratio of surface area to volume decreases, the efficiency of movement of nutrients and other other respiratory requirements into the cell and waste products out of the cell also decreases, until eventually a point is reached where it is no longer possible to move stuff in and out of the cell enough to meet the cell's requirements for survival. At this point, the organism essentially has only one of two options if it wishes (speaking metaphorically, of course) to keep growing. One is the option that our far-distant ancestors took - going multicellular, so that instead of being one large, inefficient sphere the organism can be many, more efficient spheres. The other option is arguably simpler - why stick to a sphere? Why not go filamentous? This week's highlight taxon belongs to one group of organisms that did just that - the bacterial family Streptosporangiaceae.

The filamentous option has actually been taken up by more clades of organisms than has true multicellularity. In an evolutionary sense, it's much easier - multicellular organisms require a host of measures to hold cells together and transport materials between them. Filamentous organisms, at the most basic level, simply need to grow along one geometrical axis faster than they grow along the others. Indeed, filamentous organisms rather blur the line between "multicellular" and "unicellular". Many of the larger filamentous organisms such as have cross-membranes dividing sections of hyphae, but they don't necessarily have to. Fungi and xenophyophores are both groups of organisms made up of masses of filaments, and is there any real reason other than comparative tradition for one to be regarded as multicellular and one as unicellular? (Does the concept of a "cell" even really apply when discussing hyphal organisms?) Bacteria are usually imagined as being unicellular, but many members of two bacterial groups, the cyanobacteria (blue-green algae) and the somewhat slime-mould-like Myxococcales, are multicellular for at least part of their life cycles. In contrast, the group of bacteria that made a go of the filamentous life-style was the Actinobacteria, the group to which the Streptosporangiaceae belong. Actinobacteria (or actinomycetes) include a diverse range of bacteria, both filamentous and not so (another subgroup of the Actinobacteria, the Corynebacterineae, has previously been covered here and here). Because of our shaky understanding of bacterial phylogenetics, it's difficult to say anything truly meaningful about the evolution of the filamentous habit in Actinobacteria, but it has most likely been lost and regained a number of times in the group. Some of the Actinobacteria have developed the hyphal habit to the extent that they are superficially ver similar to fungi, and indeed have been classified as such in the past.


Sporangia of Planomonospora alba. Image from Atlas of Actinomycetes.

The Streptosporangiaceae include some of the more mould-like actinobacteria. Like fungi, Streptosporangiaceae form branching, non-fragmenting hyphae. Most (but not all) members produce aerial mycelia, on the ends of which are produced the spores. Rather unusually among bacteria, the various genera can mostly be distinguished by morphological features related to the production of sporangia and arrangement of spores (Tamura et al., 2000), leading to many of them being give such names as Planomonospora or Microtetraspora. Planotetraspora, for instance, bears long, cylindrical sporangia containing four spores in a single row (Tamura & Sakane, 2004), while Acrocarpospora produces spherical or club-shaped sporangia containing coiled spore chains (Tamura et al., 2000). The distinctive appearance of Streptosporangiaceae also means that they are one of the few non-cyanobacterial prokaryote groups with an established fossil record, thanks to the description of Streptosporangiopsis from Cretaceous amber (Waggoner, 1994).

While widespread in soils around the world, the Streptosporangiaceae have often been regarded as rare compared to other groups. As methods of culturing them have improved, however, it has been suggested that Streptosporangiaceae are not so much rare as slow-growing. When soil samples are cultured in the laboratory, they are unable to compete with faster-growing taxa (Lazzarini et al., 2000), and their isolation requires the application of stressors that they can handle better than their competitors, such as heat-drying or chlorinating compounds. Despite the difficulty of culturing them, it has been suggested that doing so would be worthwhile - Streptosporangiaceae have proven a promising target in research into isolating new antibiotic compounds.

REFERENCES

Lazzarini, A., L. Cavaletti, G. Toppo & F. Marinelli. 2000. Rare genera of actinomycetes as potential producers of new antibiotics. Antonie van Leeuwenhoek 78 (3-4): 399-405.

Tamura, T., & S. Sakane. 2004. Planotetraspora silvatica sp. nov. and emended description of the genus Planotetraspora. International Journal of Systematic and Evolutionary Microbiology 54 (6): 2053-2056.

Tamura, T., S. Suzuki & K. Hatano. 2000. Acrocarpospora gen. nov., a new genus of the order Actinomycetales. International Journal of Systematic and Evolutionary Microbiology 50 (3): 1163-1171.

Waggoner, B. M. 1994. Fossil microorganisms from Upper Cretaceous amber of Mississippi. Review of Palaeobotany and Palynology 80 (1-2): 75-84.