Thursday, March 14, 2013

Extremophilic Eukaryotes

My recent post Blastocystis aux Enfers was my "literary take" on biological adaptation of intestinal parasitic protists, using Blastocystis as an example. As a parasitologist you'd come across many peculiar and shrewd biological adaptations and life cycles, and I hope to be able to give some examples in a future post. Actually, there is a parasite which is quite common in humans, maybe even just as common as Blastocystis, which is also single-celled, but which may have a much more complicated life cycle than Blastocystis, namely Dientamoeba fragilis; a colleague of mine is currently doing his PhD on Dientamoeba and he has collected multiple sources of evidence to confirm the hypothesis that this parasite is transmitted by a vector, namely pinworm, probably along the same way that Histomonas meleagridis – the cause of blackhead disease in especially turkeys – is transmitted by heterakids (which again are transmitted by parathenic hosts such as earthworms, which get eaten by turkeys, chickens, etc.). Anyway, I’ll probably get back to Dientamoeba, once his data are out.

Meanwhile, Blastocystis comes out of a very heterogeneous group of organisms called Stramenopiles, many of which are algae. Algae are photosynthetic organisms found in habitats as diverse as glacial ice and hot springs.One of these algae is named Galdieria sulphuraria, which is a remarkable unicellular eukaryote inhabiting hostile environments such as volcanic hot sulfur springs where it is responsible for about 90% of the biomass; indeed this certainly qualifies as "Galdieria aux enfers"!

Galdieria sulphuraria (source)
A research group led by Gerald Schönknecht and Andreas Weber has published a study in Science, in which they have demonstrated that this particular red alga has adapted to harsh environments through a process called horizontal (or lateral) gene transfer (HGT) which is non-sexual movement of genetic information between two organisms (eg. by virus (phages)). Bacteria and archaea commonly adapt through HGT. HGT has also been observed in some micro-eukaryotes, but the significance of this has been unclear, and for instance, there has been limited data to resolve whether HGT in micro-eukaryotes could lead to any increase in fitness.

It appears that G. sulphuraria has gained genes from extremophile bacteria by HGT. Phylogenetic analysis of ATPases found in G. sulphuraria showed that these enzymes were of archaeal origin and probably contributing to the alga's heat tolerance. Tolerance to salinity was also speculated to be a consequence of HGT. Remarkable metabolic flexibility in G. sulphuraria appears also to be a consequence of gene acquisition from both bacteria and archaea. As a last example, genes encoding arsenical resistance efflux pumps may have been acquired from thermophilic and/or acidophilic bacteria living in the same environment as the alga.

These findings are remarkable because they support the theory of gene transfer from bacteria and archaea shaping adaptational processes of extremophilic unicellular eukaryotes.

Anaerobism is another type of extremophilism. We also know that intestinal micro-eukaryotes such as Entamoeba has most likely adopted to anaerobism by secondary gene loss and HGT primarily from bacterial lineages. Blastocystis is another species that may have adapted to an anaerobic life cycle by the assistance of HGT. For instance there is evidence of genes associated with the synthesis of Fe/S clusters (which are essential to the oxidation-reduction reactions of mitochondrial transport) that may have been acquired by an ancestor of Blastocystis by HGT from a methanoarchaeon, some of which are common inhabitants of the human intestine. Recently, analysis of the Blastocystis genome revealed over 100 potential candidate genes potentially acquired by HGT from bacteria and archaea.

Some nematodes are obligate anaerobes... they can live as anaerobic parasites within the human intestine with only females reaching sexual maturity and giving birth to offspring by parthenogenesis (virgin birth), but might also thrive as free-living, sexually distinct worms: Strongyloides stercoralis.

Suggested reading:

To read about the Galdieria sulphuraria Genome Project, go here.

Schönknecht G, Chen WH, Ternes CM, Barbier GG, Shrestha RP, Stanke M, Bräutigam A, Baker BJ, Banfield JF, Garavito RM, Carr K, Wilkerson C, Rensing SA, Gagneul D, Dickenson NE, Oesterhelt C, Lercher MJ, & Weber AP (2013). Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science (New York, N.Y.), 339 (6124), 1207-10 PMID: 23471408

Keeling PJ (2009). Functional and ecological impacts of horizontal gene transfer in eukaryotes. Current opinion in genetics & development, 19 (6), 613-9 PMID: 19897356

Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, Squares R, Whitehead S, Quail MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillén N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, El-Sayed NM, Petri WA Jr, Clark CG, Embley TM, Barrell B, Fraser CM, & Hall N (2005). The genome of the protist parasite Entamoeba histolytica. Nature, 433 (7028), 865-8 PMID: 15729342

Denoeud F, Roussel M, Noel B, Wawrzyniak I, Da Silva C, Diogon M, Viscogliosi E, Brochier-Armanet C, Couloux A, Poulain J, Segurens B, Anthouard V, Texier C, Blot N, Poirier P, Ng GC, Tan KS, Artiguenave F, Jaillon O, Aury JM, Delbac F, Wincker P, Vivarès CP, & El Alaoui H (2011). Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome biology, 12 (3) PMID: 21439036

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