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

Of Interstitial Annelids (Taxon of the Week: Pisionidae)

Head end of Pisione. Photo by Greg Rouse.

The Pisionidae are tiny (about a centimetre or less in length), transparent, mostly marine annelid worms (a single species has been described from fresh water - San Martín et al., 1998). They are usually counted as members of the meiofauna, the community of minute animals (and other heterotrophic eukaryotes) that live in the spaces between sand grains, though Rouse and Pleijel (2001) quibbled with this assignation on the grounds that pisionids are too large relative to average sand grain size. Nevertheless, they are probably predators of meiofaunal organisms that they capture with their venomous jaws. About forty species of Pisionidae are currently recognised; however, in light of their ease of being overlooked, it would not be surprising if many species remain undescribed. Most pisionids are found in shallower and intertidal waters but some have been recorded at depths of up to 1000 m. The life histories of few pisionids have been studied but fertilisation is direct with males possessing paired ventral "penes" on varying numbers of segments that transfer the aflagellate sperm to the females' seminal receptacles. Larvae of the species Pisione remota are planktic feeders, capturing food by means of a mucus net.

Phylogenetic studies of Pisione remota have provided strong support for a position of pisionids among the scale worms, a clade of annelids normally characterised by the possession of paired chitinous elytra (Wiklund et al., 2005). This is supported both by molecular analysis and by similarities in the venom glands. The study of Wiklund et al. (2005) went so far as to find P. remota nested among species of the elytra-bearing family Sigalionidae and suggested that 'pisionids' may in fact be derived sigalionids (however, only a single pisionid and three sigalionids were included in the analysis so further more extensive studies are required to confirm the families' relative positions). The implied loss of the elytra in pisionids is usually suggested to be an adaptation to their infaunal habitat and small size. However, other infaunal scale worms have not lost their elytra so this may not be the entire story.

REFERENCES

Rouse, G. W., & F. Pleijel. 2001. Polychaetes. Oxford University Press.

San Martín, G., E. López & A. I. Camacho. 1998. First record of a freshwater Pisionidae (Polychaeta): description of a new species from Panama with a key to the species of Pisione. Journal of Natural History 32 (8): 1115-1127.

Wiklund, H., A. Nygren, F. Pleijel & P. Sundberg. 2005. Phylogeny of Aphroditiformia (Polychaeta) based on molecular and morphological data. Molecular Phylogenetics and Evolution 37 (2): 494-502.

Name the Bug: Polyplacus kilmeri

Close-up of plates of Polyplacus kilmeri. Figure from Wilbur (2006).

Even among the generally bizarre world of Palaeozoic echinoderms, helicoplacoids stand out as particularly wierd (see this page by Chris Mah for an overview of their wierdness). But if there was to be such a thing as a helicoplacoid family reunion then there would be one family member that even the other helicoplacoids would be looking sideways at and muttering that they were a little odd; that member would be Polyplacus.

The Helicoplacoidea were a short-lived group of animals from very early in the Cambrian period. Their overall body shape was similar to a football, or a spindle, or a sort of armour-plated turd. The ambulacral (feeding groove) arrangement was essentially Y-shaped with two upper branches and one lower branch, but this 'Y' was then wrapped around the body in a left-handed spiral. One of the upper branches stopped further away from the uppermost point than the other while the lower branch stopped some distance short of the body's lower point. Most authors regard helicoplacoids as having been sessile in life with the ambulacrum-free lower part buried into soft sediment to hold the animal upright (like a rugby ball sitting in a kickstand). The body wall was made up of a large number of small plates held together by soft tissue; the plates were not anchored to each other directly, so the animal would have been able to expand or contract as it required. However, because of this lack of direct articulation, the plates in even well-preserved fossils have invariably shifted somewhat relative to each other so that any fine-scale features, such as were the body openings were located, are obscured. A few different reconstructions of helicoplacoid anatomy have been suggested, none of which (it must be said) make a huge deal of sense. For instance, Sprinkle & Wilbur (2005) (among others) locate the mouth at the junction of the three ambulacral branches; this is the most reasonable position in comparison to the anatomy of other echinoderms but implies a lateral position for the mouth in the living animal when pretty much all other sessile animals have their mouths positioned dorsally. In contrast, Durham (1993) suggested that the mouth might be located at the upper apex which seems more sensible from a functional perspective, but implies a branching and reversal of direction in the ambulacrum that is completely unlike anything seen in any other echinoderm (and, I can't help suspecting, may be developmentally impossible).


The type specimen of Polyplacus kilmeri as figured in Durham (1967). The entire specimen is five centimetres long.

Durham (1993) recognised nine species of helicoplacoid in four genera but Wilbur (2006) recently reduced the number of species to three, regarding the diagnostic features of the remaining 'species' as due to ontogeny and/or the degree of expansion of the specimen when preserved. Two of those species, Helicoplacus gilberti and Waucobdella nelsoni, have the whorls of the ambulacra (with biserial floor-plates and flanking cover plates) divided by distinct interambulacral zones, similar to the arrangement in other echinoderms. In Polyplacus kilmeri, however, while the overall arrangement in plates is spiral as in other helicoplacoids, there are no distinguishable ambulacra. Or, to put it another way, the skeleton appears to be all ambulacra, as the interambulacral zones have been replaced by arrays of small plates identical to the ambulacra of Helicoplacus gilberti (Wilbur, 2006). The true ambulacra of Polyplacus kilmeri have not yet been identified on either of the two specimens of this species known (Wilbur, 2006, seems to allude to the possibility that Polyplacus may be a pathological monstrosity rather than a true species but unfortunately there is simple not enough material available to establish this).

The phylogenetic position of helicoplacoids relative to other echinoderms remains highly debatable. Many authors have suggested a very basal position for helicoplacoids on the basis of their overall distinctiveness and early appearance in the fossil record, suggesting that they represent a trimerous stage in echinoderm evolution that preceeded the pentamerous stage more characteristic of the phylum. Others (e.g., Sprinkle & Wilbur, 2005) regard helicoplacoid trimery as derived rather than ancestral, perhaps from the pentamerous edrioasteroids. The suggestion of Smith (1988) that helicoplacoids might even be para- or polyphyletic, with Polyplacus closer to other echinoderms than to Helicoplacus, is based on a very speculative interpretation of Polyplacus and seems highly unlikely. The unique spiral morphology of helicoplacoids seems unlikely to have arisen twice, nor does it seem likely to have given rise to more orthodox echinoderms.

REFERENCES

Durham, J. W. 1967. Notes on the Helicoplacoidea and early echinoderms. Journal of Paleontology 41 (1): 97-102.

Durham, J. W. 1993. Observations on the early Cambrian helicoplacoid echinoderms. Journal of Paleontology 67 (4): 590-604.

Smith, A. B. 1988. Patterns of diversification and extinction in early Palaeozoic echinoderms. Palaeontology 31 (3): 799-828.

Sprinkle, J., & B. C. Wilbur. 2005. Deconstructing helicoplacoids: reinterpreting the most enigmatic Cambrian echinoderms. Geological Journal 40: 281-293.

Wilbur, B. C. 2006. Reduction in the number of Early Cambrian helicoplacoid species. Palaeoworld 15 (3-4): 283-293.

More in the Bloodsucking Vein (Taxon of the Week: Simulium)

Female Simulium feeding. Photo by maz_nat.

Blackflies of the genus Simulium (including several hundred species - see Adler & Crosskey, 2008, for a listing if you're really keen) are found around the world and familiar to most people for their blood-sucking habits. Like other members of the fly clade Culicomorpha, such as mosquitoes and chironomid midges, the larvae of blackflies are aquatic filter-feeders while only the females feed on blood as adults. In fact, blackflies (like other culicomorphs) are primarily nectar- rather than blood-feeders. Both males and females feed on nectar as adults and the females may require only a single blood meal to complete development of their eggs (Cupp & Collins, 1979).


Simulium larvae in a stream. The close-up photo is of the head of a filter-feeding larva. Photo from here.

Which is not to say that the role of blackflies as parasites is negligible. Askew (1971) refers to a plague of Simulium columbaschense in 1923 causing the deaths of nearly 20,000 head of livestock along the banks of the Danube. The most notorious blackflies are members of the Simulium damnosum complex of Africa (with one species, S. rasyani, in Yemen) which carry the human-parasitic worm Onchocerca volvulus. As well as the debilitating skin disease infection with Onchocerca causes in the majority of cases, approximately 250,000 people are rendered blind by Onchocerca infections every year. The various species of the Simulium damnosum complex are largely indistinguishable externally and require examination of their chromosome arrangements to be identified; however, different species differ significantly in their potential as Onchocerca vectors. Some 55 'species' have been identified in the complex, making it one of the largest known assemblages of cryptic species (Post et al., 2007).

REFERENCES

Adler, P. H., & R. W. Crosskey. 2008. World blackflies (Diptera: Simuliidae): a fully revised edition of the taxonomic and geographical inventory. http://blackflies.info/sites/blackflies.info/files/u13/blackflyinventory_2008_Adler___Crosskey_1.pdf. Accessed 23 March 2010.

Askew, R. R. 1971. Parasitic Insects. Heinemann Educational Books: London.

Cupp, E. W., & R. C. Collins. 1979. The gonotrophic cycle in Simulium ochraceum. American Journal of Tropical Medicine and Hygiene 28 (2): 422-426.

Post, R. J., M. Mustapha & A. Krueger. 2007. Taxonomy and inventory of the cytospecies and cytotypes of the Simulium damnosum complex (Diptera: Simuliidae) in relation to onchocerciasis. Tropical Medicine and International Health 12 (11): 1342-1353.

Name the Bug # 14

Possibly the most evilly difficult ID challenge I've put up yet (unless you've seen this particular figure before, perhaps) but trust me, it's so worth it. The scale bar represents 1 mm. Attribution, as always, to follow.

Update: Identity now available here. Figure from Wilbur (2006).

The Hard Way to be a Bloodsucker (Taxon of the Week: Ixodidae)

A mature gorged female of Ixodes ricinus, the sheep tick or castor bean tick, ready to lay her eggs. Photo by Jarmo Holopainen.

Ticks are probably the most familiar of all mite groups. Not only do they include by far the largest mite species but they also feed on the blood of vertebrates, a habit guaranteed to bring them to our attention. The ticks themselves would usually be more irritating than dangerous, except on occasions when they attack in large numbers, but many ticks are vectors of some very unpleasant diseases. Ticks are classified into three families of which the largest is the Ixodidae or hard ticks with a little under 700 species (Horak et al., 2002). Hard ticks are distinguished from members of the Argasidae or soft ticks by the presence of a hardened scutum at the front of the dorsum (the third tick family contains a single species, the African Nuttalliella namaqua). In males the scutum can cover almost the entire dorsal surface while the female scutum is restricted to the front part of the body over the legs. Hard ticks also have the capitulum (the 'head') directed forward so that it is easily visible from above while soft ticks have the capitulum pointed downwards (Nicholson et al., 2009).


A female of the cattle tick Rhipicephalus microplus laying her not inconsiderable brood of eggs. Photo from here.


Cattle ticks removed from a single calf. Photo from here.

The hard tick life cycle contains four stages of a single instar each - egg, larva, nymph and mature adult (soft ticks have multiple nymphal instars). Eggs are laid in large clusters of hundreds or thousands - the record number of eggs laid by a single female is 34,000 for a specimen of Amblyomma variegatum (Nicholson et al., 2009). Like other mites, larval ticks have only six legs when they first hatch out; the fourth pair doesn't appear until the nymphal stage. In both the larval and nymphal stages the young ticks will find a suitable host and feed then usually drop off and moult away from the host* (a small number of species don't leave the host before moulting and remain on a single host for their entire life). Some tick species are very choosy about their hosts (the best-known of which being the cattle tick, Rhipicephalus microplus [aka Boophilus microplus]) while others such as the sheep tick Ixodes ricinus are far more catholic. Some species feed on different hosts at different life stages. Even if suitable hosts are few and far between, some ticks can survive for over a year without feeding while they wait for one to turn up (some soft ticks can survive for several years without food). Males of Ixodes do not feed after reaching maturity and usually mate with females before they attach themselves to the final host (though some may mate on the host) while mature males of other ixodid genera do feed and copulation between the sexes takes place on the host (all together now - ewww). After copulation, the attached female gorges herself on her host's blood, swelling up to many times her original size. Once her eggs are mature, she drops off the host, lays her eggs in a suitable sheltered site, and dies (in contrast, female soft ticks can find another host and mate with another male, eventually surviving for several years).

*I have to admit to being surprised when I learnt that ticks didn't just latch onto their final host right away, even though in retrospect it should have been bloody obvious. After all, they would hardly be as much concern as disease vectors if they only ever attacked a single individual.


Back when she was skinny - a female lone star tick Amblyomma americanum sitting on vegetation waiting for a host. Photo by James Gathany.

Phylogenetic analysis supports a basal division in Ixodidae between Ixodes and other genera which is consistent with the differences in life cycles between the two groups (Murrell et al., 2003).

REFERENCES

Horak, I. G., J.-L. Camicas & J. E. Keirans. 2002. The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): a world list of valid tick names. Experimental and Applied Acarology 28: 27-54.

Murrell, A., N. J. H. Campbell & S. C. Barker. 2003. The value of idiosyncratic markers and changes to conserved tRNA sequences from the mitochondrial genome of hard ticks (Acari: Ixodida: Ixodidae) for phylogenetic inference. Systematic Biology 52 (3): 296-310.

Nicholson, W. L., D. E. Sonenshine, R. S. Lane & G. Uilenberg. 2009. Ticks (Ixodida). In Medical and Veterinary Entomology, 2nd ed. (G. R. Mullen & L. A. Durden, eds) pp. 483-532. Academic Press.

Quick Question: What Would You Bring Back?

I just came across this post at a blog called Zygoma that asks the question: if you could bring any organism back from extinction, what would you choose and why? My first choice would be a stylophoran such as Cothurnocystis in order to resolve the anatomy of those very confusing fossils. Close runners-up would be Helicoplacus (for the same reason as Cothurnocystis) or Mazothairos (for the sheer glory of Awesome) or Homo erectus (in a probably futile attempt to shake that nasty idea of human exceptionalism held by too many people). Or maybe I should just get myself some Tullimonstrum, grow them up to enormous sizes and release them into Scottish lakes.

So what would you choose and why?

A Small Bag of Grains (Taxon of the Week: Saccamminidae)

Tests of the agglutinating foram Saccammina sphaerica. Scale bar = 500 μm. These are the lectotype and paralectotype of this species held by the British Natural History Museum.

Foraminifera are one of the best-known of protist groups and may make up more than half of the benthic biomass in some marine habitats, particularly in the deep sea (Gooday et al., 2001). Forams are amoeboids with filose pseudopodia that branch and rejoin each other to form a net for the collection of food particles. The great majority of forams are marine, and most (but not all) forams produce some sort of protective test or shell with the filopodia extending from openings or pores in the test. Because of this test, forams are one of the few protist groups with an extensive fossil record. Indeed, their use in biostratigraphic studies (and leading surveyors to small treats such as oil deposits) has lead to forams being better known from a palaeontological than a Recent perspective and the structure and morphology of the test has long been a major factor in distinguishing and classifying forams.

Forams may secrete their own tests (usually chitinous or calcareous) or they may construct a test from sand grains and/or other foreign particles (these are known as agglutinating forams). A distinction is also commonly made between monothalamous forms, in which the test is not divided into chambers (at least, not by complete septa), and polythalamous forms, in which the test is divided by septa into a number of chambers. However, molecular phylogenetic studies of recent forams have shown that monothalamous forams are paraphyletic while polythalamous forms are potentially polyphyletic (Flakowski et al., 2005). Also, while monothalamous taxa may produce chitinous or agglutinated tests, the type of test produced does not appear to correspond with phylogenetic position (Pawlowski et al., 2002).

Despite this, foram researchers continue to use the old test-based classification for the simple reason that no-one has yet come up with a better alternative (and doing so would not be easy). The Saccamminidae as generally recognised are a large family of agglutinating forams with generally a single chamber (or sometimes a bunch of similar chambers loosely attached to each other), usually with a single aperture. They may be globular or more elongate in shape. Some saccamminids are quite catholic in their choice of building materials but others may be more fussy. Perhaps the ultimate in fussiness is expressed by Technitella thompsoni which builds its test with nothing but the ambulacral plates of brittle stars (Cushman, 1940).


The 'silver saccamminid', an as-yet unidentified species that has appeared in a number of phylogenetic studies. Photo by Jan Pawlowski.

As with other monothalamous groups, molecular phylogenetic studies have indicated that "saccamminids" are polyphyletic with representative species scattered in various positions among the basal part of the foram tree (Cedhagen et al., 2009; Gooday & Pawlowski, 2004). Despite a fossil record extending back to the Cambrian (with putative 'saccamminids' at least as far back as the Silurian) and a significant abundance in the modern marine benthos, agglutinating forams are not as well-studied as calcareous taxa and monothalamous forms are particularly poorly so. For a start, they are often extremely small. Ecological studies have found the majority of 'saccamminid' specimens to be much less than 100 μm in diameter (Gooday et al., 2001) though Pilulina jeffreysii reaches more than 4 mm (Cedhagen et al., 2009). Also problematic, particularly for palaeontological studies, is that agglutinating foram tests are often difficult to distinguish from their surrounding environment because they are, after all, made from their surrounding environment. Perhaps the best demonstration of this issue is that the Stannomidae, despite being the largest of all forams and reaching over a foot in size, have no recognised fossil history at all.

REFERENCES

Cedhagen, T., A. J. Gooday & J. Pawlowski. 2009. A new genus and two new species of saccamminid foraminiferans (Protista, Rhizaria) from the deep Southern Ocean. Zootaxa 2096: 9-22.

Cushman, J. A. 1940. Foraminifera: their classification and economic use, 3rd ed. Harvard University Press: Cambridge (Massachusetts).

Flakowski, J., I. Bolivar, J. Fahrni & J. Pawlowski. 2005. Actin phylogeny of Foraminifera. Journal of Foraminiferal Research 35 (2): 93-102.

Gooday, A. J., H. Kitazato, S. Hori & T. Toyofuku. 2001. Monothalamous soft-shelled Foraminifera at an abyssal site in the North Pacific: a preliminary report. Journal of Oceanography 57: 377-384.

Gooday, A. J., & J. Pawlowski. 2004. Conqueria laevis gen. and sp. nov., a new soft-walled, monothalamous foraminiferan from the deep Weddell Sea. Journal of the Marine Biological Association of the UK 84 (5): 919-924.

Pawlowski, J., M. Holzmann, C. Berney, J. Fahrni, T. Cedhagen & S. S. Bowser. 2002. Phylogeny of allogromiid Foraminifera inferred from SSU rRNA gene sequences. Journal of Foraminiferal Research 32 (4): 334-343.