|
ScienceWeek
EVOLUTION: ON PLACOZOA -- THE SIMPLEST KNOWN ANIMAL
The following points are made by D.J. Miller and E.E. Ball (Current Biology 2005 15:R26):
1) Often described as the simplest known animal, the unassuming marine placozoan Trichoplax adhaerens is one of a handful of "lower" metazoans that have so far defied being pigeonholed. The history of Trichoplax and its relatives has the elements of a scientific mystery story [1]. In 1971, Karl Grell [2] formally described a new Phylum, the Placozoa, to accommodate two species that had been reported a hundred years earlier. These were originally greeted with excitement as "living fossils" representing the ancestral animal morphology. However, the suggestion that they were, in fact, modified cnidarian larvae prompted a loss of interest for the next fifty years. One of the species upon which Placozoa was founded, Treptoplax reptans, has never been seen since its original description, and is assumed not to exist; T. adhaerens, on the other hand, appears to be widely distributed and relatively common in warm marine environments [1]. However, other than field surveys [3], all that is known about it is based on aquarium cultures.
2) Although T. adhaerens was until now the sole recognized species in the phylum Placozoa, the levels of molecular heterogeneity reported by Voigt et al.[4] imply that what has previously been considered one species may actually be several. Cryptic molecular diversity thus underlies the apparently uniform morphology of placozoans and, as the majority of the cell biological studies to date have been based on a single isolate from the Red Sea, this study highlights the need for further research on this enigmatic group of animals.
3) In culture, individual Trichoplax are flat and irregular disc-like animals a few millimeters in diameter (environmental isolates are often smaller) and 10-15 microns thick. Although molecular studies point to additional cellular complexity, Trichoplax has been repeatedly described as comprising just four cell types arranged in three layers - an upper and a lower epithelium separated by the "fiber cell". The latter has a syncytial organization and its contractile properties are often assumed to be responsible for the amoeba-like changes in shape. The upper layer consists of monociliated "cover" cells, whereas two cell types make up the lower epithelium -- gland cells, which are non-ciliated and thought to secrete digestive enzymes, and ciliated "cylinder" cells that may be adhesive and capable of resorbing digestion products [1].
4) Little is known about the natural diet of Trichoplax, although it is assumed to consist of micro-algae and organic detritus. In culture, they have been maintained for years on a diet of Cryptomonas, which are more or less dissolved upon contact with the gland cells. The morphology of the cylinder cells indicates that they are responsible for uptake of the dissolved nutrients. Trichoplax sometimes elevate their center from the substrate to form one or more digestive bags, and on glass substrates they frequently leave behind an area that is cleared of everything edible.
5) In summary: A recent report of high levels of genetic variation between strains of Trichoplax adhaerens challenges the traditional view that the phylum Placozoa comprises only one species. At the morphological level, placozoans are amongst the simplest extant animals, but molecular evidence suggests that they may have more complex origins.
References (abridged):
1. Grell, K.G. and Ruthman, A. (1991). Placozoa. In Microscopic Anatomy of Invertebrates, Vol.2: Placozoa, Porifera, Cnidaria and Ctenophora. Harrison, F.W. and Westfall, J.A. eds. (New York: Wiley-Liss), pp. 13-27
2. Grell, K.G. (1971). Trichoplax adhaerens: F.E. Schulze und die Entstehung der Metazoen. Naturwiss. Rundschau 24, 160-161
3. Maruyama, Y.K. (2004). Occurrence in the field of a long-term, year-round, stable population of placozoans. Biol. Bull. 206, 55-60
4. Voigt, O., Collins, A.G., Buchsbaum Pearse, V., Pearse, J.S., Ender, A., Hadrys, H. and Schierwater, B. (2004). Placozoa: no longer a phylum of one. Curr. Biol. 14, R944-R945
5. Collins, A.G. (2002). Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J. Evol. Biol. 15, 418-432
Current Biology http://www.current-biology.com
--------------------------------
Related Material:
BIOEVOLUTON: PROTOZOAN-METAZOAN HORIZONTAL GENE TRANSFER
The following points are made by R.E. Steele et al (Current Biology 2004 14:R298):
1) Horizontal gene transfer has been well documented as a significant feature of genome evolution in prokaryotes [1-3]. The frequency and significance of this process in eukaryotic evolution is much less clear. Confirming that a gene has entered a species by a horizontal route can be difficult, and many previously reported cases of horizontal gene transfer from a prokaryote to a eukaryote have subsequently been invalidated [4]. Because of potential contamination, extra care must be taken when putative horizontal gene transfers are detected in sequence datasets from organisms that may harbor a significant number of parasites and commensals.
2) In a small number of metazoan phyla, a significant fraction of the mRNA contains a leader sequence that is attached by trans-splicing [5]. These spliced leaders are distinct for each phylum and thus provide a tag that can be used to determine the origin of a trans-spliced mRNA. Thus, presence of a spliced leader on a mRNA from a trans-splicing species would confirm that the gene was not derived from a non trans-splicing contaminating organism.
3) Hydra, a member of the basal phylum Cnidaria, is one of the few metazoan taxa in which trans-spliced leaders are added [5]. In a large EST (expressed sequence tag) project with Hydra magnipapillata (www.hydrabase.org), the authors have identified a cDNA homologous to the flp genes of the parabasalid protist Trichomonas vaginalis. The flp1 and flp2 genes of T. vaginalis are of unknown function, but their expression is dramatically down-regulated in response to increasing levels of iron. A third flp gene (flp3) was identified by searching the unfinished T. vaginalis genome sequence with the flp1 and flp2 sequences. The flp genes are not found in any other EST dataset, nor are they found in any of the other sequenced genomes. The flp gene is conspicuously absent from the genome datasets of other protists (e.g., Plasmodium falciparum, Giardia lamblia, Tetrahymena thermophila macronuclear genome, and the Entamoeba histolytica genome).
4) The anomalous phylogenetic distribution of flp suggests that this gene has been horizontally transferred [1]. The preferred approach for testing such a hypothesis is phylogenetic analysis with an appropriate outgroup species. However, the limited occurrence of the flp gene makes such an analysis impossible. An alternative explanation for the distribution of flp genes is that they were ancestrally present in all eukaryotes and secondarily lost from most taxa. However, this seems unlikely as the large amount of sequence available for diverse taxa did not reveal flp genes. Rather, it seems most likely that the flp gene was horizontally transferred. The direction of transfer is at present uncertain. The authors favor the idea of transfer from a parabasalid protist to a cnidarian, but the authors suggest additional information on the distribution of flp genes in parabasalid protists and cnidarians will be required to resolve this question.
References (abridged):
1. Philippe, H. and Douady, C.J. (2003). Horizontal gene transfer and phylogenetics. Curr. Opin. Microbiol. 6, 498-505
2. Eisen, J.A. (2000). Horizontal gene transfer among microbial genomes: new insights from complete genome analysis. Curr. Opin. Genet. Dev. 10, 606-611
3. Jain, R., Rivera, M.C., Moore, J.E., and Lake, J.A. (2002). Horizontal gene transfer in microbial genome evolution. Theor. Popul. Biol. 61, 489-495
4. Genereux, D.P. and Logsdon, J.M.Jr. (2003). Much ado about bacteria-to-vertebrate lateral gene transfer. Trends Genet. 19, 191-195
5. Nilsen, T.W. (2001). Evolutionary origin of SL-addition trans-splicing: still an enigma. Trends Genet. 17, 678-680
Current Biology http://www.current-biology.com
--------------------------------
Related Material:
EVOLUTIONARY BIOLOGY: ON METAZOAN EVOLUTION
The following points are made by F. Raible and D. Arendt (Current Biology 2004 14:R106):
1) It is a truism that the plausibility of an evolutionary inference increases with the amount of data on which it is based, and the ever-quickening provision of full genome sequences is providing a huge amount of grist for the evolutionary biologist's mill. Genome data are now available for man, mouse, fish, tunicates, nematodes and flies, and their comparison shows that a large proportion of genes are shared across all the Bilateria --the animals with bilateral symmetry. But such comparisons also, of course, reveal phylogenetically relevant differences. What were the molecular changes that accompanied the evolution of the major bilaterian branches -- the vertebrates in particular --from their last common ancestors, the Urbilateria?[1].
2) While it is clear that the duplication of existing genes has played a major role in vertebrate evolution [2], the contribution of novel genes to the rise of the vertebrate lineage remains ill-defined. Current estimates from our chordate relative, the tunicate Ciona intestinalis, claim that as many as one sixth of its genes could represent evolutionary innovations shared only with the vertebrates [3]. But a series of recent studies [4,5] reveal that many of the supposedly vertebrate/chordate-specific genes instead have a long evolutionary history.
3) Genes found in only one of the sequenced genomes, but not in others, have naturally been considered evolutionary novelties. This follows the parsimonious view that a gene that is found, for example, in the human genome but not in that of the fruitfly Drosophila or nematode Caenorhabditis elegans, should have arisen on the evolutionary line leading to humans. New studies, however, indicate that this view is too simplistic; it seems, rather, that we still possess many genes that were lost on the lineages leading to Drosophila and C. elegans, and can be traced back to pre-bilaterian times or even stem-line metazoans. A more complete sampling of transcriptomes across the Metazoa, in the form of "expressed sequence tag" (EST) collections, indicates that, in assessing potential evolutionary innovations on the vertebrate lineage, we have been misled by the rapid rate of molecular evolution, with large gene losses, of the invertebrate model species.
4) In summary: Comparison of newly available sequence data facilitates reconstruction of the gene inventory of the Urbilateria, the last common ancestors of flies, nematodes and humans. The most surprising outcome is that human genes seem to be closer to the bilaterian roots than previously assumed.
References (abridged):
1 De Robertis, E.M. and Sasai, Y. (1996). A common plan for dorsoventral patterning in Bilateria. Nature 380, 37-40
2 Levine, M. and Tjian, R. (2003). Transcription regulation and animal diversity. Nature 424, 147-151
3 Dehal, P., Satou, Y., Campbell, R.K., Chapman, J., Degnan, B., De Tomaso, A., Davidson, B., Di Gregorio, A., Gelpke, M., and Goodstein, D.M. et al. (2002). The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298, 2157-2167
4 Kortschak, R.D., Samuel, G., Saint, R., and Miller, D.J. (2003). EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol. 13, 2190-2195
5 Krylov, D.M., Wolf, Y.I., Rogozin, I.B., and Koonin, E.V. (2003). Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res. 13, 2229-2235
Current Biology http://www.current-biology.com
ScienceWeek http://scienceweek.com
|