Dictyotales

Most of the various 'seaweeds' found around the world can be assigned to one of three major groups, each named for their most characteristic pigments: green algae, red algae and brown algae. Of these, green algae are the closest relatives of land plants, and red algae are the most taxonomically diverse. But for many people, the most familiar of the three will be brown algae. Owing to their often relatively large size and predilection for growing in visible locations, brown algae are likely to be the first examples to come to mind when one thinks of seaweed. For this post, I'm examining a particular subgroup of the brown algae, the family Dictyotaceae.

Forkweed Dictyota dichotoma, copyright Ria Tan.

Representatives of the Dictyotaceae can be found around the world but are more diverse in warmer tropical and subtropical waters. They seem to be particularly diverse in the Australasian region. Dictyotaceae are moderately sized seaweeds with flattened thalli that may grow as branching ribbons or radiating fans. One fan-shaped species of Dictyotaceae, Padina pavonica, has earned itself the vernacular name of 'peacock's tail'(this species is also notable for being one of the few calcified brown algae). These thalli grow apically from meristematic cells. Dictyotaceae have an isomorphic life cycle with the alternating sexually and asexually reproducing generations being similar in overall appearance. Sporangia in asexual individuals grow as superficial nodules scattered over the surface of the thallus; the resulting spores usually differ from those of other brown algae in lacking flagella. The less abundant sexual individuals are mostly divided between separate males and females (Bittner et al. 2008).

Peacock's tail Padina pavonica, copyright Diego Delso.

Dictyotaceae are distinct enough from other brown algae to have consistently been treated as their own order (indeed, their sporangia are unique enough that some very early authors did not even regard them as brown algae). Two species found around Australasia, Dictyotopsis propagulifera and Scoresbyella profunda, have previously been considered distinct enough to warrant their own separate families within this order Dictyotales. Dictyotopsis propagulifera has a monostromatic thallus (that is, the thallus is only one layer of cells thick). Scoresbyella profunda has an apical growing cell that divides lengthwise to the thallus instead of transversely as in other Dictyotales. However, molecular data have indicated that these two genera are nested within Dictyotaceae and so only the single family is currently recognised. Dictyotaceae has also been divided in the past between tribes Dictyoteae and Zonarieae based on the nature of the apical growing cells (Dictyoteae have a single meristematic cell whereas Zonarieae have a cluster or row of cells) and some authors have even treated them as distinct families. Again, however, molecular data have not corroborated this division (Bittner et al. 2008).

Lobophora variegata, copyright John Turnbull.

For most species of Dictyotaceae, their greatest significance to humans probably comes from the role they play in providing habitats to fish and other marine animals. As with other algae, Dictyotaceae produce a range of secondary metabolites that serve functions such as protecting them from grazers, and some of these may prove to have economic applications. Some species of Dictyotaceae, on the other hand, have become significant invasive species. A dramatic recent example has been provided by the northern Pacific species Rugulopteryx okamurae which was probably first imported to the Mediterranean as a contaminant on farmed oysters (García-Gómez et al. 2020). This species was recorded on the southern coast of France in 2002 and was later recorded on the coast of Ceuta in 2015. Within a year of the latter record, its presence in Ceuta had reached absolute plague proportions. Most of the illuminated rocky sea bottom was covered by R okamurae, up to about 90% coverage at optimal depths about ten to twenty metres. Over 5000 tons of washed-up seaweed was removed from the beaches of Ceuta in 2016. Needless to say, native seaweeds, and other sessile marine organisms such as corals, would have been severely impacted by this spread.

Rugulopteryx okamurae in Morocco, from El Aamri et al. (2018).

What caused this dramatic invasion? It would have certainly been a factor that defensive metabolites produced by Rugulopteryx okamurae had a negative impact on competitors. But perhaps even more significant a factor was climate change. Rising sea temperatures in the Straits of Gibraltar would have made things uncomfortable for native marine life used to cooler conditions. Meanwhile, the subtropical immigrant would have found things increasingly to its liking. With its competition hobbled and nothing to hold it back, R. okamurae was set to take over.

REFERENCES

Bittner, L., C. E. Payri, A. Couloux, C. Cruaud, B. de Reviers & F. Rousseau. 2008. Molecular phylogeny of the Dictyotales and their position within the Phaeophyceae, based on nuclear, plastid and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution 49: 211–226.

García-Gómez, J. C., J. Sempere-Valverde, A. R. González, M. Martínez-Chacón, L. Olaya-Ponzone, E. Sánchez-Moyano, E. Ostalé-Valriberas & C. Megina. 2020. From exotic to invasive in record time: the extreme impact of Rugulopteryx okamurae (Dictyotales, Ochrophyta) in the strait of Gibraltar. Science of the Total Environment 704: 135408.

Naviculi, Navicula

Diatoms are one of the most prominent groups of micro-algae in aquatic environments, perhaps more abundant than any other major group of aquatic organisms except bacteria. As such, they are a key component in many of the environmental processes that we ultimately depend on: food for aquatic animals, producers of oxygen, et cetera et cetera. To those who study them, they are also known for the intricate architecture of their silica walls. As well as being aesthetically pleasing, this architecture forms a key component of diatom classification. One of the most diverse groups of diatoms recognised has been the mega-genus Navicula.

Light microscope view of Navicula tripunctata, copyright Kristian Peters.

Historically, over one thousand species have been assigned to Navicula. Though more recent authors have restricted the name to a smaller, more tightly defined concept than before, it still contains some 200 or so species (Bruder & Medlin 2008). Species assigned to this genus are an elongate diamond or pill shape. Though the term 'navicula' can be translated from Latin as a small boat, and this is often assumed to be the name's origin, this is incorrect. Its original author, the French naturalist Jean-Baptiste Geneviève Marcellin Bory de Saint-Vincent, derived the name from the French term for a weaver's spindle (navette de tisserand; Cox 1999). A long fissure, the raphe, runs down the midline of each valve of the diatom wall; the diatom moves by extruding secretions through the raphe. In Navicula, the raphe is largely straight though it may be hooked at the ends of the valve. Perpendicular to or radiating from the raphe are striae formed of rows of openings (areolae); in Navicula, these areolae are more or less elongate with their long axes perpendicular to the line of the stria. In some species historically included in Navicula, the striae may be biseriate with two rows of areolae. Some authors have proposed recognising species with biseriate striae as a distinct genus Hippodonta. Cox (1999) disputed whether this distinction was enough to warrant a separate genus but Bruder & Medlin (2008) conducted a molecular phylogenetic analysis of naviculoid diatoms in which the one Hippodonta species included was placed as the sister taxon to Navicula sensu stricto. In distinguishing the genus Sellaphora from Navicula, Mann (1989) also identified a number of cytoplasmic features characteristic of Navicula sensu stricto, such as the possession of two distinct plastids per cell with rod-like pyrenoids.

SEM view of Navicula dobrinatemniskovae, from Van de Vijver et al. (2011). Scale bar = 1 µm.

Ecologically, the majority of species of Navicula sensu stricto (about 150 species) are found in freshwater environments (Bruder & Medlin 2008). In temperate and tropical regions, they are a diverse element of benthic diatom communities, but they are less predominant in coldwater habitats (Van de Vijver et al. 2011). They are most characteristic of meso- to eutrophic lakes and permanent waterways and Van de Vijver et al. (2011) therefore suggested that they might be less suited for the damp soils and temporary pools that dominate freshwater habitats in the frozen South. Nevertheless, these authors still managed to identify five previously unknown species from just this inhospitable region, giving some indication of what still remains to be discovered of this already diverse genus.

REFERENCES

Bruder, K., & L. K. Medlin. 2008. Morphological and molecular investigations of naviculoid diatoms. III. Hippodonta and Navicula s. s. Diatom Research 23 (2): 331–347.

Cox, E. J. 1999. Studies on the diatom genus Navicula Bory. VIII. Variation in valve morphology in relation to the generic diagnosis based on Navicula tripunctata (O. F. Müller) Bory. Diatom Research 14 (2): 207–237.

Mann, D. G. 1989. The diatom genus Sellaphora: separation from Navicula. British Phycological Journal 24 (1): 1–20.

Van de Vijver, B., R. Zidarova, M. Sterken, E. Verleyen, M. de Haan, W. Vyverman, F. Hinz & K. Sabbe. 2011. Revision of the genus Navicula s.s. (Bacillariophyceae) in inland waters of the sub-Antarctic and Antarctic with the description of five new species. Phycologia 50 (3): 281–297.

Getting Your Diatoms in a Row

Diatoms are one of the world's primary groups of aquatic unicellular algae. Perhaps only the cyanobacteria rival them for ecological significance. They play a crucial role in the production and fixation of nutrients on which other organisms depend.

Colony of Melosira moniliformis attached to some sort of weed, copyright Frank Fox. The last individual seems to have suffered some unfortunate bisection.

Diatoms live protected in a siliceous test or, to put it another way, they really do live in glass houses. The test is composed of a pair of opposed valves; as noted by Round & Crawford (1990), the arrangement of valves is commonly compared to that of a Petri dish. The valves themselves do not overlap directly in the manner of a Petri dish, but a series of girdle bands around the edge of each valve does overlap. Diatoms come in a range of shapes and structures (artistically minded microscopists [or microscopically minded artists, however you wish to phrase it] have been known to create kaleidoscopic patterns through the careful arrangement of diatoms on a slide) and have commonly been divided between two major groups on the basis of the main symmetry of the valves. Centric diatoms have valves that are radial in appearance when viewed from above whereas pennate diatoms have elongated, more bilateral valves.

Melosira is a widespread genus of centric diatoms found in both fresh and salt water. It might be considered the classic centric: the test is circular in dorsal view and rectangular in side view so the overall shape is that of a hat box. Individual cells remain united by pads of mucilage following division, resulting in the formation of long chains. Species of the genus differ in their preferred habitats. One freshwater species, Melosira varians, is commonly found in polluted or poor quality waters. Conversely, a marine species M. arctica is the most abundant algal species known from the Arctic Ocean, responsible for nearly half the Arctic's primary production. Diatoms lack flagella for most of their life cycle (only their gametes are ever flagellate) so they are not active swimmers. In life, they are either found attached to a substrate or, if floating as planktonic, suspended in the water column by turbulence. One species, M. italica, is known to survive in sediment during quiescent periods of the year and resume growth when winter turbulence returns it to the light (Round & Crawford 1990).

Auxospores of Melosira varians, copyright Kristian Peters.

When diatom cells divide, each daughter cell receives one of the parent's original test valves and secretes a new valve to match it. As noted above, the marginal girdles of the valves overlap, and the new valve is always secreted as the inner partner of this overlap. As a result, and because the glass valves cannot change in size once secreted, successive generations of diatom cells become inexorably smaller over time. Obviously, this process cannot continue indefinitely least the cells dwindle to extinction, so sexual reproduction plays a vital role in resetting the process of diatom development. Centric diatoms like Melosira produce distinct gamete types, motile spermatozoids and immobile eggs (in contrast, many pennate diatoms produce only a single gamete type with no such distinction). Zygotes produced from the fusion of these gametes grow into a cell called an auxospore that differs from normal diatom cells in possessing a organic cell covering instead of solid glass valves. This organic covering may be reinforced with individual siliceous scales, but some Melosira auxospores remain contained and protected within the valves of their parent and lack scales of their own (Medlin & Kaczmarska 2004). The auxospore will not produce a uniform glass test until it has reached full mature size; in Melosira this initial test differs from the standard in being globular rather than pillbox-shaped. The auxospore will then begin dividing into daughter cells in the usual well which will themselves produce test valves of the standard shape. But each of the auxospore's daughters, of course, will receive one of it's initial valves, so as the Melosira chain develops it will remain hemispherical at each end.

REFERENCES

Medlin, L. K., & I. Kaczmarska. 2004. Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia 43 (3): 245-270.

Round, F. E., & R. M. Crawford. 1990. Phylum Bacillariophyta. In: Margulis, L., J. O. Corliss, M. Melkonian & D. J. Chapman (eds) Handbook of Protoctista. The structure, cultivation, habitats and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. A guide to the algae, ciliates, foraminifera, sporozoa, water molds, slime molds and the other protoctists pp. 574–596. Jones & Bartlett Publishers: Boston.

A Western Rockweed

Rockweed Silvetia compressa, from here.

Silvetia compressa is a species of brown alga found on shorelines on the western coast of North America, from British Columbia to Baja California. It is a member of the wrack family Fucaceae that I covered in an earlier post. Silvetia compressa is found in midtidal habitats, generally higher up on the shoreline than other large seaweeds. Individual thalli can reach a maximum length of about three feet (90 cm) but are often smaller. This is a slow-growing species, so patches of Silvetia are slow to recover from damage due to trampling and other disturbance. Please try to avoid walking on the rockweed!

Thalli of Silvetia compressa are composed of thin strands a few millinetres in width with irregular, dichotomous branching. Strands of the thalli lack a midrib (distinguishing them from some other Fucaceae species found in the same area). The width of the strands and regularity of the branching varies with environmental conditions: for instance, individuals growing in locations with stronger wave action have more robust strands that branch more frequently. As with other Fucaceae, the reproductive structures a produced on swollen branch tips called receptacles, but these receptacles do not become inflated with gases and buoyant like those of other species. The exact size and shape of the receptacles is, again, variable.

In many older references, Silvetia compressa may be referred to as Pelvetia fastigiata. The supposed species 'Fucodium compressum' and 'F. fastigiatum' were originally distinguished on the basis that the latter was smaller than the former with more fastigiate branches (that is, the branches remained subparallel). As indicated above, these characters represent the effects of environmental conditions, not fixed differences (Silva 1996). They were eventually included in the genus Pelvetia, together with the Atlantic species P. canaliculata, on the basis of the thalli without a midrib, and the production of just two eggs from each oogonium in the receptacles. However, later analyses supported the separation of the Atlantic and Pacific species of Pelvetia. Not only did they not form a clade in molecular analyses, the eggs in the oogonia were separated by a horizontal division in the Atlantic species but a longitudinal or oblique division in the Pacific species (Silva et al. 2004). As such, the Pacific Pelvetia were transferred into a new genus Silvetia.

Further taxonomic complications involved subspecific variation in Silvetia compressa. A distinctive form of 'Pelvetia fastigiata' found at Pebble Beach in California's Monterey Bay, with smaller, finer thalli and more abundant, regular branching, was labelled as a separate forma gracilis. Similar individuals were also found on the islands off California's coast. However, when Silva (1996) examined the original type specimen of P. fastigiata, he discovered that it was an individual of this 'gracilis' form, not the more typical larger form. Later, Silva et al. (2004) examined genetic variation within the Silvetia compressa of California and Baja California. They found that the individuals of the offshore islands were indeed genetically distinct from continental individuals. As well as the differences in growth habit, there was also some difference in receptacle shape: the continental form had receptacles that tended to be linear and pointed whereas those of the island form were ellipsoidal and blunt. However, the island form still could not be labelled with either of the 'fastigiata' or 'gracilis' monikers, as individuals from the type locality of Pebble Beach did not align genetically with insular individuals but with other continental forms. As such, yet another name had to be coined for the insular form which now goes by the name of Silvetia compressa ssp. deliquescens. Let's see if it sticks this time.

REFERENCES

Silva, P. C. 1996. California seaweeds collected by the Malaspina expedition, especially Pelvetia (Fucales, Phaeophyceae). Madroño 43 (3): 345–354.

Silva, P. C., F. F. Pedroche, M. E. Chacana, R. Aguilar-Rosa, L. E. Aguilar-Rosa & J. Raum. 2004. Geographic correlation of morphological and molecular variation in Silvetia compressa (Fucaceae, Fucales, Phaeophyceae). Phycologia 43 (2): 204–214.

The Wracks

Bladder wrack Fucus vesiculosus, from here.

'Wrack' is one of those lovely old-fashioned words that doesn't get used anywhere near as often as it deserves. As well as being an alternative for the word 'wreck' (such as in The Wrack of Hesperus), it refers to a number of larger brown seaweeds, including the subjects of today's post, the Fucaceae.

The Fucaceae are dichotomously branching seaweeds mostly found in the intertidal zone. They vary in size from smaller forms growing higher in the littoral zone (such as the 15-cm-or-less Pelvetia fastigiata) to quite large forms growing lower down (the mid-littoral Ascophyllum nodosum may have fronds two metres in length). Fucaceae are distinguished from other families of brown algae by features such as their well-defined apical and marginal receptacles, and the single four-sided apical cell on each frond (Cho et al. 2006). Fucaceae also differ from some other brown algae in lacking a free-growing haploid stage in their life cycle: haploid cells do undergo a few rounds of post-meiotic mitosis within the receptacles, but are released as individual eggs and sperm that immediately fuse to found the diploid generation.

With the removal of the Australasian Xiphophoraby Cho et al. (2006), the Fucaceae has become a strictly Northern Hemisphere family. This is interesting because the larger clade of the Fucales to which the Fucaceae belong is mostly Southern Hemisphere in diversity. Representatives of the Fucaceae are found both in the Pacific and the Atlantic, with a distinct flora in each (only a single species, Fucus distichus, is believed to be native to both oceans, though some would separate the Pacific population as F. gardneri). Cánovas et al. (2011) favoured a Pacific origin for the Fucaceae, on the grounds that this provided the most intuitive biogeographical connection to the related Australasian taxa Xiphophora and Hormosira, but parsimony analysis alone was unable to confirm or deny this scenario. Basal clades within the family include representatives in both oceans.

The North Pacific Silvetia compressa, photographed by James Watanabe.

Though currently divided between six genera, the family is not speciose, and only two of those genera include more than a single species: the Pacific Silvetia (three species; previously included in Pelvetia but removed by Serrão et al. 1999 on the grounds of non-monophyly) and the mostly Atlantic Fucus (eight[?] species). The clade may be fairly recent in origin: though estimating an age is complicated by the relatively poor fossil record of brown algae, Cánovas et al. (2011) estimated with molecular dating that the Fucaceae diverged in the mid to late Miocene, with their ancestors possibly crossing the equator as Australia moved north. Complicating matters, species of Fucaceae can be morphologically very variable: in the 1960s, for instance, H. T. Powell revised the 100+ species, varieties and forms then recognised within Fucus down to only six species (Serrão et al. 1999). These species can be divided between a northern, specifically cold-water clade with the rockweed Fucus distichus and the toothed wrack F. serratus, and a more warm-water-tolerant clade containing the remaining species (Cánovas et al. 2011). These species tend to be ecologically distinct, each preferring slightly different microhabitats within the littoral zone, but they can hybridise where they come into contact and reproductive isolation is probably not complete (Zardi et al. 2011). Two further species of Fucus have been recognised recently: F. guiryi is a north-eastern Atlantic species previously recognised as F. spiralis var. platycarpus (Zardi et al. 2011; the name 'Fucus platycarpus' cannot be used for this species owing to homonymy), while F. radicans is a species unique to the relatively low-salinity Baltic Sea (Bergström et al. 2005). All indications are that Fucus radicans is a recent segregate from the more widespread bladder wrack F. vesiculosus, which is also the only other Fucus species found in the Baltic. The Baltic Sea itself is not, in its current form, very old, and molecular data suggest that the divergence of F. radicans may have only happened within the last four hundred years (Pereyra et al. 2009).

Knotted wrack Ascophyllum nodosum, from Fisheries and Oceans Canada.

REFERENCES

Bergström, L., A. Tatarenkov, K. Johanneson, R. B. Jönsson & L. Kautsky. 2005. Genetic and morphological identification of Fucus radicans sp. nov. (Fucales, Phaeophyceae) in the brackish Baltic Sea. Journal of Phycology 41: 1025-1038.

Cánovas, F. G., C. F. Mota, E. A. Serrão & G. A. Pearson. 2011. Driving south: a multi-gene phylogeny of the brown algal family Fucaceae reveals relationships and recent drivers of a marine radiation. BMC Evolutionary Biology 11: 371.

Cho, G. Y., F. Rousseau, B. de Reviers & S. M. Boo. 2006. Phylogenetic relationships within the Fucales (Phaeophyceae) assessed by the photosystem I coding psaA sequences. Phycologia 45 (5): 512-519.

Pereyra, R. T., L. Bergström, L. Kautsky & K. Johannesson. 2009. Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea. BMC Evolutionary Biology 9: 70.

Serrão, E. A., L. A. Alice & S. H. Brawley. 1999. Evolution of the Fucaceae (Phaeophyceae) inferred from nrDNA-ITS. Journal of Phycology 35: 382-394.

Zardi, G. I., K. R. Nicastro, F. Canovas, J. Ferreira Costa, E. A. Serrão & G. A. Pearson. 2011. Adaptive traits are maintained on steep selective gradients despite gene flow and hybridization in the intertidal zone. PLoS One 6 (6): e19402.

Algal Threads (Taxon of the Week: Myrionemataceae)

Discs of Myrionema strangulans on a blade of Ulva lactuca. Photo from here.

The brown algae of the Phaeophyceae* are one of the predominant groups of multicellular algae in the modern ocean. Though not the most speciose of the three (that title belongs to the red Macrorhodophytina), they are in many places the most ecologically significant, as this is the group that includes the gigantic kelps that predominate and shape many parts of the marine environment. As significant as kelps are, though, they are not my focus for today. Instead, I'm going to look at a much smaller group of brown algae, the Myrionemataceae.

*The names "Phaeophyceae" or "Phaeophyta" have usually been used to refer to the monophyletic clade of multicellular brown algae. Cavalier-Smith & Chao (2006) recently proposed an expanded "class Phaeophyceae" to include the unicellular Phaeothamniophyceae and the very-basically-multicellular Schizocladia, with the traditional Phaeophyceae referred to as "subclass Melanophycidae". As Cavalier-Smith & Chao did not dispute the monophyly of the traditional Phaeophyceae, this is a simple ranking issue and I suspect it will probably be largely ignored by everyone else.

Myrionemataceae are minute filamentous algae, usually only a couple of millimetres in size (Abbott & Hollenberg, 1993). They generally grow in a disc only one or two cells deep, with numerous filaments growing upwards from the strands of the disc. These filaments may be uniserial or branching; they may or may not carry lateral processes or sporangia. Myrionemataceae most commonly seem to be epiphytic on much larger marine plants and algae.


Close-up of Microspongium globosum, an Atlantic myrionematoid alga. Image from Taşkin et al. (2006).

Myrionemataceae (and small filamentous brown algae in genera) have been a royal pain in the neck for algal taxonomists, and as a result they have been widely shunned. For instance, the main distinguishing characteristic between the Myrionemataceae and the similarly filamentous Ectocarpaceae has been that the former is discoidal and the latter is not (Clayton, 1974). However, the genus Hecatonema (included by some authors in Myrionemataceae and excluded by others) includes some species that always grow in a disc, and others that do not. Some "Myrionemataceae" have been suggested to represent divergent growth forms or dimorphic generations of other brown algae placed in different families (many marine algae have very distinct alternating generations). This seems very probable for some species, but proving such relationships is not easy and Clayton (1972) claimed that at least some cases of myrionematoid algae being grown from cultures of other algae represented contamination instead of relationship. Other Myrionemataceae that have been cultured show no signs of alternating generations, while yet others have only ever been recorded reproducing asexually.


Individual filament of Myrionema strangulans, showing close-up structure. From DeCew's Guide.

It seems almost certain that the "Myrionemataceae" are a polyphyletic grouping, with their overall lack of distinguishing features obscuring a diversity of origins. Peters (2003) found the type genus, Myrionema, to be itself polyphyletic. The type species of Myrionema, M. strangulans, has a fairly isolated position within the Ectocarpales sensu lato in Draisma et al. (2001), but it is pretty much anyone's guess as to how many of the so far unanalysed myrionematoid species belong with it*. Some species may be established as growth-forms of other taxa and shipped off accordingly, but others may prove more intractable and remain in the "family" - not so much a wastebasket as an inedible core.

*Das et al. (2005), in a paper that had me completely baffled but which I rather suspect was complete twaddle to begin with, cite a later phylogeny which they attribute to Draisma et al. (2002) that positions Myrionema strangulans in the Chordariaceae - unfortunately, Draisma et al. (2002) has absolutely no mention anywhere of Myrionema, chordariaceous or otherwise, so I wouldn't know what reference Das et al. really had in mind.

REFERENCES

Abbott, I. A., & G. J. Hollenberg. 1993. Marine Algae of California. Stanford University Press.

Cavalier-Smith, T., & E. E.-Y. Chao. 2006. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). Journal of Molecular Evolution 62: 388-420.

Clayton, M. N. 1972. The occurrence of variant forms in cultures of species of Ectocarpus and Giffordia. Br. phycol. J. 7: 101-108.

Clayton, M. N. 1974. Studies on the development, life history and taxonomy of the Ectocarpales (Phaeophyta) in southern Australia. Australian Journal of Botany 22: 743-813.

Das, S., J. Chakrabarti, Z. Ghosh, S. Sahoo & B. Mallick. 2005. A new measure to study phylogenetic relations in the brown algal order Ectocarpales: The “codon impact parameter”. J. Biosci. 30: 699–709.

Draisma, S. G. A., J. L. Olsen, W. T. Stam & W. F. Prud'homme van Reine. 2002. Phylogenetic relationships within the Sphacelariales (Phaeophyceae): rbcL, RUBISCO spacer and morphology. European Journal of Phycology 37: 385-401.

Draisma, S. G. A., W. F. Prud'homme van Reine, W. T. Stanm & J. L. Olsen. 2001. A reassessment of phylogenetic relationships within the Phaeophyceae based on RUBISCO large subunit and ribosomal DNA sequences. Journal of Phycology 37: 586-603.

Peters, A. F. 2003. Molecular identification, distribution and taxonomy of brown algal endophytes, with emphasis on species from Antarctica. In Seventeenth International Seaweed Symposium (A. R. O. Chapman, R. J. Anderson, V. J. Vreeland & I. R. Davison, eds) pp. 293-302. Oxford University Press.

Taşkin, E., M. Öztürk & M. J. Wynne. 2006. First report of Microspongium globosum Reinke (Phaeophyceae, Myrionemataceae) in the Mediterranean Sea. Nova Hedwigia 82 (1-2): 135-142.

Return of the Slime-nets

Another milestone has been reached in the Catalogue of Organisms - this will be the first Taxon of the Week post where the taxon in question has already been covered in the series. So what group of organisms is illustrious enough to be worth introducing twice? In this case, that honour goes to the Labyrinthulea, the slime-nets, and I don't think you could find a more deserving target. The biggest challenge, I suspect, will be finding enough good images online to illustrate to post - for some reason, good labyrinthulean images seem to be a little thin on the ground.


Vegetative cells of Labyrinthula terrestris within epidermis of Poa trivialis. Scale bar = 10 µm. Photo from Bigelow et al. (2005).

In my previous post on labyrinthuleans, I introduced you all to the group and gave a brief rundown of their division into three morphological if not necessarily phylogenetic groups, the labyrinthulids, thraustochytrids and the Diplophrys group. I recommend reading that post before this one, but this time round I'd like to focus more on the ecological role of Labyrinthulea. As alluded to in the previous post, the vast majority of known labyrinthuleans are marine, a habitat in which they appear to be pretty much ubiquitous (Raghukumar, 2002). It is thought that within the marine habitat labyrinthuleans mostly act as decomposers, living by breaking down and extracting nutrients from dead plant, algal and animal matter. They are very effective in this role - for instance, thraustochytrids are capable of breaking down sporopollenin, the extraordinarily resistant polymer that coats pollen grains. However, because labyrinthuleans in such a role have little direct effect on humans (though their significance to nutrient cycles vital to other organisms that are significant to humans is probably considerable), this is not how they have been most studied. Instead, much more attention has been given to their interactions with living organisms as commensals or pathogens.

Despite numerous records of labyrinthuleans as pathogens, it seems likely that in the majority of cases they are not primarily so, but merely facultative. Despite their rapid growth on necrotic algal tissue, growth of thraustochytrids on live algae is minimal or non-existent, even when said algae have been deliberately innoculated with thraustochytrid spores. Raghukumar (2002) postulated that antimicrobial substances produced by healthy plants might effectively keep thraustochytrid growth down. Labyrinthulids are somewhat more aggressive in their relationships with marine plants and algae, but are not necessarily harmful - the species Aplanochytrium minutum, for instance, has been recorded living within the tissues of brown algae without any noticeable adverse effects on the host. Thraustochytrids are also known as pathogens of animals - in many cases, the effects of thraustochytrid infection are not severe except in young animals, but the QPX organism that has caused mass mortality in the clam Mercenaria mercenaria has been shown using molecular means to belong to the thraustochytrids.


Lottia alveus, the seagrass-inhabiting limpet driven to extinction by the seagrass wasting disease epidemic of the 1930s. Reconstruction from here.

A dramatic exception to the generally low-key nature of labyrinthulean pathogenicity reared its ectoplasm in the 1930s. In the early part of that decade, a wasting disease of then-unknown cause devastated populations of the seagrass Zostera marina in the North Atlantic. More than 90% of the seagrass beds on both sides of the Atlantic were wiped out. In some places, the effect was so severe that the ecology of the area affected was completely altered and the seagrass never returned (Short et al., 1987). The indirect effects of this devastation on other organisms, needless to say, were also severe. Migratory waterfowl populations declined, while several commercial fisheries were hard hit - in particular, the scallop fishery on the American eastern seaboard collapsed entirely. At least one species dependent on the seagrass, the limpet Lottia alveus, became extinct as a result of the epidemic. By the 1940s, the epidemic had run its course, and seagrass populations began to recover by the 1950s. The reasons for the wasting disease remained unknown, though it was suggested that abnormally high sea temperatures may have been a factor. It wasn't until a smaller scale outbreak of seagrass wasting disease in 1986 that Short et al. (1987) were able to show that it was caused by a Labyrinthula species. While the cataclysmic levels of the 1930s have never, thankfully, returned, wasting disease remains a concern for the maintenance of seagrass populations.


Grass infected with rapid blight. Photo by D. Bigelow.

It is a pathogenic species that also provides the sole exception yet known to the otherwise entirely aquatic lifestyle of Labyrinthulea. Rapid blight of cool season lawn turf was first described in California as recently as 1995, and has since been recorded from multiple locations across the southern United States. Once again, the identity of the causative organism was difficult to resolve, but it was eventually described as a new species of Labyrinthula in 2005. How a representative of an otherwise exclusively marine genus came to be parasitising grass in a terrestrial environment remains a complete unknown, though Bigelow et al. (2005) suggested that Labyrinthula may be more common in soil than previously thought, but overlooked due to the difficulty in culturing it.

REFERENCES

Bigelow, D. M., M. W. Olsen & R. L. Gilbertson. 2005. Labyrinthula terrestris sp. nov., a new pathogen of turf grass. Mycologia 97 (1): 185-190.

Raghukumar, S. 2002. Ecology of the marine protists, the Labyrinthulomycetes (thraustochytrids and labyrinthulids). European Journal of Protistology 38 (2): 127-145.

Short, F. T., L. K. Muehlstein & D. Porter. 1987. Eelgrass wasting disease: cause and recurrence of a marine epidemic. Biological Bulletin 173 (3): 557-562.

Slime Nets: Another Group of Not-Fungi

The subject of this week's Taxon of the Week post is another example of the under-rated nature of protist diversity. Labyrinthuleans, commonly referred to as 'slime nets' are one of those organisms that, being neither animals nor plants, have been shuffled back and forth between and within the nomenclatural codes over the years, resulting in the same taxon being referred to by multiple different names. Labyrinthulea, Labyrinthista and Labyrinthulomycota are just three options that might be encountered. They are one of the protist groups that have been described as 'slime moulds', though they lack the dramatic life cycles of the Mycetozoa, the slime moulds proper. Most labyrinthuleans are found in aquatic habitats, but some species are terrestrial.

Labyrinthuleans may be divided into three groups, the Thraustochytriales, Labyrinthulales and the Diplophrys group. Note that these may not be phylogenetically separate groups - the molecular analysis of Cavalier-Smith & Chao (2006), for instance, doesn't separate the three - but they are still useful form groups. The Labyrinthulales and Thraustochytriales are united by the possession of an organelle called a bothrosome or sagenogen(etosome) that produces large amounts of filamentous net-like ectoplasmic membrane that the individual cells move along and absorb nutrients through, hence the name of 'slime nets'. The image at the top of this post (from here) shows a colony of Labyrinthula on the left and a close-up of individual cells on the right. Many labyrinthuleans are parasitic and invade and break down cells of host organisms, absorbing nutrients released by the decomposing cells. The individual cells form aggregative masses during reproduction, within which enlarged cells undergo meiosis and release flagellated zoospores (Barnes, 1998). The most obvious difference between the two groups seems to be the mode of colony formation - while Labyrinthulales form dispersed colonies of loosely connected cells surrounded by ectoplasmic matrix as seen in the top photo, Thraustochytriales (as exemplified in the photo of Schizochytrium limacinum below, again from here) form more compact colonies with the ectoplasmic net growing as "roots" from the base of the colony. The small inset photo shows the zoospore of Schizochytrium.



The genera Diplophrys and Sorodiplophrys are associated with the labyrinthuleans by molecular (Cavalier-Smith & Chao, 2006) and ultrastructural (Dykstra & Porter, 1984) data. However, while they do produce and move on ectoplasmic outgrowths, they lack a bothrosome for the production of said ectoplasm. Zoospore production has also never been recorded for these genera. The terrestrial Sorodiplophrys has an aggregative stage in its life cycle, but the aquatic Diplophrys marina does not (the actual type species of Diplophrys, D. archeri, has not been observed since 1902, and D. marina is only tentatively included in the same genus). Interestingly, the analysis of Cavalier-Smith & Chao (2006) places Diplophrys marina within the Labyrinthulales, which if correct implies that it lost the labyrinthulean characteristics during its evolutionary history.

As 'slime moulds', the labyrinthuleans were originally regarded as fungi (hence some publications refer to them as labyrinthulomycetes). However, it is now universally agreed that they are in fact members of the heterokonts (Chromista) based on the ultrastructure of the zoospores, as well as molecular data. Within the heterokonts, Cavalier-Smith & Chao (2006) place labyrinthuleans in a basal heterotrophic clade that also includes bicoecids and opalozoans and is sister to the remaining heterokonts. Labyrinthuleans are therefore not even close relatives of the other "ex-fungal" chromists in the Pseudofungi.

Labyrinthuleans have relatively little economic significance to humans. Some labyrinthuleans attack hosts of economic significance to humans, such as bivalves or golf course turf. Oils from the thraustochytrialean Schizochytrium contain one of the current dietary buzzwords, omega-3 fatty acids, so commercial growth of Schizochytrium is used to produce dietary supplements and alternatives to fish oils. Interestingly, webpages, patents, articles, etc. referring to such uses of Schizochytrium seem to invariably refer to it, somewhat misleadingly, as an 'alga', and the product as 'algal oil'. This strikes me as only a marginal improvement over 'fungus'.

REFERENCES

Barnes, R. S. K. 1998. The Diversity of Living Organisms. Blackwell Publishing.

Cavalier-Smith, T., & E. E.-Y. Chao. 2006. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). Journal of Molecular Evolution 62: 388-420.

Dykstra, M. J., & D. Porter. 1984. Diplophrys marina, a new scale-forming marine protist with labyrinthulid affinities. Mycologia 76 (4): 626-632.

Giant Cannibal Algae from the Watery Ditch

I didn't think I was going to post anything today - nothing had really grabbed my attention over the last couple of days to write about. But then I look in my e-mail and find a notice about something I really couldn't resist - giant cannibal algae!

Chrysophytes (also known as "golden algae" due to the colour of their chloroplasts) are a class of unicellular algae found in pretty much any aquatic habitat. Your average chrysophyte is not particularly prepossessing - a single cell with one or two flagella emerging from one end and a scattering of chloroplasts within the cell. The image at the top of the post (from here) shows a couple of individuals of one such chrysophyte, Ochromonas. Some chrysophytes produce a covering lorica or coating of scales, while some live in small gelatinous colonies. Chrysophytes can produce resistant statospores or cysts when conditions become unfavourable (in at least some species, this may be induced by increasing population density rather than external environmental conditions), and as a result active populations of chrysophytes often show marked cycles between bloom and quiescent periods. The spore structure of chrysophytes is unique to this group, with a wall composed mostly of silica opening through a collared pore plugged with polysaccharides. Almost all chrysophytes can become heterotrophic (feeding on other organisms) if light conditions are not good enough for photosynthesis, and a number of chrysophytes have ditched chloroplasts altogether and are obligate heterotrophs.

A paper just out today by Yubuki et al. (2008) describes the life cycle of one such colourless chrysophyte, belonging to the genus Spumella. I wasn't able to find a picture of Spumella on the web, but if you imagine Ochromonas without chloroplasts you won't be too far off. Unfortunately, the organisms concerned are not identified to species. This could potentially be a problem as Spumella may be polyphyletically derived from chrysophyte lines that have independently lost chloroplasts (Cavalier-Smith & Chao, 2006). Whatever the species examined actually was, it was recovered from an ephemeral ditch where it would have had to survive periods of drying out.

The single cell that hatched out through the pore of a resistant spore was initially non-motile, but soon sprouted flagella and started to swim. It then produced a gelatinous sphere around itself, which it continued to swim in. The cell then started reproducing by binary cell division at a rapid rate (doubling time at 22°C was about two and a half hours), with the growing cells feeding on bacteria growing within the matrix of the gelatinous sphere, which continued to increase in size as the number of inhabiting cells increased. Eventually, after about two days, the sphere broke down, releasing the swimming cells into the surrounding medium.

Some hours after leaving the sphere, the cells began congregating in swarms of up to forty individuals. It was then that things turned nasty. Some cells within the swarm began capturing others and engulfing them*. Growth of these cannibal cells was rapid, and they soon became two or three times the size of their unfortunate siblings. Finally, the enlarged cannibal cells dropped their flagella and produced their own dormant cysts, waiting for the next stage in the cycle.

*If you can access the original paper, there's an absolutely fantastic sequence of photos of this. You can practically hear the cannibal cell smacking its lips (if it had them) after swallowing its sibling.


Figure from Yubuki et al. (2008), showing the life cycle of Spumella.

The first remarkable thing about this cycle was how quickly it all happened - from initial hatching to re-encystment took only three days. This rapidity is probably an adaptation to the unstable habitat that the organism lives in - reproduction and encystment has to be complete by the time the water supply dries up. The gelatinous matrix inhabited by the growing cells seems to facilitate this rapid life cycle by encouraging the growth of bacteria and providing the cells with a ready food supply (offhand, such a gelatinous matrix in which the cells are free-swimming has previously been described from only a single other organism - another chrysophyte, Chromulina nebulosa). The cannibalism within the swarm may also serve the same purpose. Cannibalism has been recorded in other protist species, but seems in those cases to be an opportunistic response to disappearing food supplies. In Spumella, cannibalism may be obligate - when individuals of two other protist species, Bodo and Ochromonas, both comparable in size to the cannibalised Spumella, were added to the medium, they were completely ignored and the cannibal Spumella continued to feed only on members of their own species.

Chomp.

REFERENCES

Cavalier-Smith, T., & E. E.-Y. Chao. 2006. Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). Journal of Molecular Evolution 62 (4): 388-420.

Yubuki, N., T. Nakayama, & I. Inouye. 2008. A unique life cycle and perennation in a colorless chrysophyte Spumella sp. Journal of Phycology 44 (1): 164-172.

Parcelling plastids

The Table of Contents alert for a bright, shiny new issue of Protist arrived in my e-mail box today. This is a journal I can usually rely on to supply something worthy of note (often some things), and today's was no exception. Right near the beginning of the issue, we receive a new class of heterokont (Horn et al., 2007).

So many new chromist classes have appeared in recent years that they're almost becoming routine (see Filling in the Gaps for another post of mine on one, which also includes an overview of the heterokonts). Today's subject has been dubbed Synchromophyceae, and contains a single new species, Synchroma grande, scraped off marine rocks on the coast of the Canary Islands (perhaps not the most unpleasant place to do field work). Synchroma is a photosynthetic amoeboid that forms a meroplasmodium (a network of individual cells connected by branching and anastomosing [fusing together where they meet] reticulopodia). Meroplasmodial forms are extremely rare in chromists - the only other chromist that exhibits this body form is the haptophyte Reticulosphaera japonensis (Cavalier-Smith et al., 1996). The main cell body is contained in a flattened lorica, which is adpressed to the substrate and is more or less circular on a flat surface. In reproduction, one daughter cell remains sessile in the lorica, while the other is released as a migratory cell. Migratory and floating cells are fusiform, with axopodia extending from the anterior and posterior ends. Sessile cells could also spontaneously convert to migratory cells by hatching out of their lorica. At no stage in the life-cycle were flagella present.

Phylogenetic analysis of Synchroma demonstrated that it is part of the Ochrophyta, the photosynthetic heterokont clade. Both rbcL and 18S rDNA maximum likelihood trees placed Synchroma as sister to the Chrysophyceae + Synurophyceae clade, but support in both cases was relatively low. The absence of a girdle lamella in Synchroma's chloroplasts supports its exclusion from either of those two classes.

The most interesting feature of Synchroma, however, lies in the arrangement of chloroplasts in the cell. As I mentioned previously, the chromist chloroplast is believed to be derived from an endosymbiotic red alga in a secondary endosymbiosis. As a result, the chromist chloroplast is surrounded by four membranes that represent (from the inside out) the original cyanobacterium's external cell membrane, the vacuolating membrane of the primary host, the primary host's external cell membrane, and the vacuolating membrane of the secondary host. There is some debate about whether the chloroplasts of all chromist groups (and those of their putative sister group, the alveolates) derive from a single endosymbiotic event, or have been independently derived from multiple events. The majority of authors currently favour the former option, or at least that the number of events was quite few. However, Synchroma has a unique arrangement of chloroplasts in regard to surrounding membranes. Each individual chloroplast is surrounded by two membranes, and then multiple chloroplasts are clustered in packages contained by the remaining two membranes. Horn et al. suggest in passing that Synchroma may preserve an ancestral stage in the endosymbiotic process, after the loss of the eukaryotic endosymbiont's nucleus but before the separation of the endosymbiont's chloroplasts (after all, there is no reason why the eukaryotic endosymbiont would have necessarily had only one chloroplast per cell). In light of the derived position of Synchroma within the chromists, if this is indeed an ancestral state it makes the idea of a single endosymbiosis event rather unlikely, because this would require that the ancestral state was lost repeatedly in all other chromist groups. However, I feel that it is much more likely that the other explanation suggested by Horn et al. for Synchroma's unusual chloroplasts is correct - that it is a derived state resulting from an abnormal division pattern. The possibility that within chromists cryptophytes, haptophytes and heterokonts have gained their chloroplasts independently is not completely unbelievable, but the idea that multiple hterokont groups have done the same seems to be pushing it a little. Especially as all members of this undoubtedly monophyletic clade possess red algal-derived chloroplasts - if they derived them independently, why shouldn't at least some have green algal chloroplasts?

REFERENCES

Cavalier-Smith, T., M. T. E. P. Allsopp, M. M. Häuber, G. Gothe, E. E. Chao, J. A. Couch & U.-G. Maier. 1996. Chromobiote phylogeny: the enigmatic alga Reticulosphaera japonensis is an aberrant haptophyte, not a heterokont. European Journal of Phycology 31 (3): 255-263.

Horn, S., K. Ehlers, G. Fritzsch, M. C. Gil-Rodríguez, C. Wilhelm & R. Schnetter. 2007. Synchroma grande spec. nov. (Synchromophyceae class. nov., Heterokontophyta): an amoeboid marine alga with unique plastid complexes. Protist 158 (3): 277-293.

Filling in the gaps

I'm going to continue on with the algal theme here, because I keep getting reminded lately of neat examples. However, I'm going to take a great leap sideways and deal with a different group from rhodophytes. I'm moving towards the brown algae (sort of...)

It is universally accepted these days that the algae are a polyphyletic grouping, at least from the viewpoint of nuclear and cytoplasmic ancestry. Chlorophyll originally developed within the blue-green algae, actually a clade of bacteria (Cyanobacteria). Chloroplasts in eukaryotes then arose through endosymbiosis between a non-photosynthetic protist and a cyanobacterium. However, many authors now agree that there was probably only one such primary endosymbiosis event that led to the majority of modern chloroplasts (there is a lonely cercozoan*, Paulinella, that appears to have derived its chloroplast independently). The direct descendants of this lucky protist today are the green plants and algae (Viridiplantae), the red algae (Rhodophyta) and a small group of unicells called the blue-green algae (Glaucophyta). Red and blue-green algae both have only a single chlorophyll type, chlorophyll a, while green algae possess a second form as well, chlorophyll b (interestingly, a small handful of cyanobacteria also possess chlorophyll b, and molecular phylogenies show that these oddjobs are not closely related within the cyanobacteria). The remaining algae are derived from secondary symbioses, where a eukaryotic alga has become an endosymbiont of another eukaryote followed by loss of the endosymbiont's independence and genetic material. This is rather spectacularly demonstrated by two secondary algal groups, the chlorarachneans and cryptophytes, whose chloroplasts retain a highly-reduced eukaryotic nucleus between the membranes surrounding the chloroplast. Two groups, the amoeboid chlorarachneans and flagellate euglenoids, have chloroplasts derived from green algae as shown by their possession of chlorophyll b. Four groups, the dinoflagellates, cryptophytes, haptophytes and ochrophytes, have chloroplasts seemingly derived from red algae. These four groups also share a third chlorophyll type, chlorophyll c, as well as the ancestral chlorophyll a, and on this basis it has been suggested that they all derive from a single endosymbiotic ancestor (though this seems likely, the case is not airtight as there are a number of non-photosynthetic protists without chloroplasts that seem to be closely related to one or another of the chlorophyll c groups). Some dinoflagellates have replaced their ancestral chloroplasts with chloroplasts derived from haptophytes in a tertiary endosymbiosis.

*Originally I had identified Paulinella in this post as an amoebozoan, but it belongs to a different amoeboid group, the Cercozoa.

Multicellularity has evolved a number of times within algae. Viridiplantae became multicellular multiple times, while red algae probably evolved multicellularity once at the base of the Bangiophyceae + Florideophyceae clade (see the previous post). Ochrophytes include two groups of multicellular algae, the brown algae (Phaeophyceae) and some members of the yellow-brown algae (Xanthophyceae).

Ochrophytes are the clade of photosynthetic heterokonts. Heterokonts are a well-supported clade of protists distinguished in most members by, among other features, a shorter posterior flagellum and a longer anterior flagellum with numerous side bristles (mastigonemes). At cell division, the anterior flagellum moves backwards and loses the mastigonemes to become the posterior flagellum, while a new anterior flagellum is generated (Andersen, 2004). As well as the two above-mentioned classes, ochrophytes include diatoms and a whole bunch of unicellular algae previously united as the golden algae (chrysophytes). The chrysophytes have proven to be paraphyletic with regard to the other ochrophytes, and have been divided into a whole host of smaller classes.

Now we've gotten through all that, I'll finally introduce the star of today's post, Schizocladia ischiensis Henry, Okuda & Kawai in Kawai, Maeba et al., 2003. The position of the brown algae in relation to other ochrophytes has been obscured by the absence of clear connecting features between the multicellular brown algae and the various unicellular golden algae. The significance of Schizocladia is that it goes some way towards filling that gap. Schizocladia is a small marine ochrophyte that grows as filaments of cells in single file. Like phaeophytes, Schizocladia has cell walls impregnated with alginates. Unlike brown algae, Schizocladia lacks cellulose or plasmodesmata (cytoplasmic connections between cells). Propagation in Schizocladia was via zooids produced in individual compartments in swollen cells at the end of the filaments.

The molecular phylogenies presented in the original description of Schizocladia agreed in positioning it as the sister group of Phaeophyceae. They also agreed with the result found by other studies that there is a clade composed of Phaeophyceae (+ Schizocladia), Xanthophyceae and the unicellular Phaeothamniophyceae (the unicellular Chrysomeridales may also belong to this clade, but do not appear to have been investigated molecularly). While the Xanthophyceae do include some multicellular members, it also includes unicellular forms, and multicellularity was probably evolved independently of Phaeophyceae. Xanthophyceae do possess cellulose in the cell walls, and the presence of alginates has also been demonstrated in some species.

Due to the absence of some supposed key phaeophyte characters, Schizocladia was not included in Phaeophyceae but placed in its own independent class Schizocladiophyceae. Nevertheless, its simple morphology provides a nice connection between the unicellular ochrophytes and multicellular phaeophytes.

REFERENCES

Andersen, R. A. 2004. Biology and systematics of heterokont and haptophyte algae. American Journal of Botany 91 (10): 1508-1522.

Kawai, H., S. Maeba, H. Sasaki, K. Okuda & E. C. Henry. 2003. Schizocladia ischiensis: a new filamentous marine chromophyte belonging to a new class, Schizocladiophyceae. Protist 154: 211-228.