Evidence for Geographic Isolation and Signs of Endemism within a Protistan Morphospecies

Abstract

The possible existence of endemism among microorganisms resulting from and preserved by geographic isolation is one of the most controversial topics in microbial ecology. We isolated 31 strains of "Spumella-like" flagellates from remote sampling sites from all continents, including Antarctica. These and another 23 isolates from a former study were characterized morphologically and by small-subunit rRNA gene sequence analysis and tested for the maximum temperature tolerance. Only a minority of the Spumella morpho-and phylotypes from the geographically isolated Antarctic continent follow the worldwide trend of a linear correlation between ambient (air) temperature during strain isolation and heat tolerance of the isolates. A high percentage of the Antarctic isolates, but none of the isolates from locations on all other continents, were obligate psychrophilic, although some of the latter were isolated at low ambient temperatures. The drastic deviation of Antarctic representatives of Spumella from the global trend of temperature adaptation of this morphospecies provides strong evidence for geographic transport restriction of a microorganism; i.e., Antarctic protistan communities are less influenced by transport of protists to and from the Antarctic continent than by local adaptation, a subtle form of endemism.One hot debate in microbial ecology deals with the geographic restriction of protistan taxa (8, 10-12, 22, 29). Some researchers believe that free-living protistan species are essentially ubiquitous and grow wherever suitable habitats exist. They assume that the microbial community found in any given habitat is a function of habitat properties only and not of historical factors, since there is an ubiquitous "seed bank." They further argue that geographic barriers to protists do not exist and consequently cannot contribute to evolutionary diversification (10,(12)(13)(14)(15).The basic assumption that microorganisms are easily dispersed across the physical and geographic barriers that halt the migrations of larger animals and plants (12) is, however, controversial and relies largely on the observed ubiquity of morphospecies. It has been challenged by other researchers, who believe that protists have a biogeography that has been shaped by geographic barriers (8, 30). The discussion has initiated much recent research into the existence of endemic species (10,16,28,38). However, even the definition of a species is controversial, and the low resolution of the morphospecies concept for protists appears to be an obstacle to the settling of the debate (32).Fortunately, increasing evidence for phylogenetic and ecophysiological differentiation below the morphospecies level (4,21,22,26,29,38) can theoretically be used to solve the question of possible endemism among protists. If there were no geographic barriers to protists, correlations between the habitat temperature, as a factor selecting certain strains from the seed bank, and the temperature tolerance of these strains should be independent of the geographic location. ...

Structuring effects of climate-related environmental factors on Antarctic microbial mat communities

“…Although we acknowledge that our dataset represents only a crosssection of the biodiversity of east Antarctic lakes, both eukaryotic and cyanobacterial communities are structured by geographical factors, after environmental variables are factored out. This, together with the relatively high amount of cyanobacterial sequences that have no relatives from non-Antarctic environments in GenBank, and the presence of Antarctic endemics in at least 3 other taxonomic groups, namely diatoms , flagellates (Boenigk et al 2006) and green algae (De Wever et al 2009), appears to contradict previous claims that for microorganisms "everything is everywhere" (Baas Becking 1934). Our results thus suggest that Antarctic microbial communities are probably structured by the same processes as those occurring in macroorganisms, as has been observed in studies of global diatom communities (Vyverman et al 2007).…”

“…This is likely due to the fact that the SSU rDNA is insufficient to discriminate to the species level because of its low taxonomic resolution. In fact, previous studies reported a relatively high number of endemics belonging to a variety of eukaryotic taxonomic groups (Barnes et al 2006, Gibson et al 2006b), such as diatoms , Esposito et al 2006, nematodes (Bamforth et al 2005), ciliates (Petz et al 2007), mites and springtails (Convey & Stevens 2007), flagellates (Boenigk et al 2006) and recently also green algae (De Wever et al 2009). …”

Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs Sanger insights into species richness

“…The debate over the degree to which protist communities exhibit global distribution has not been fully resolved (Foissner, 1999(Foissner, , 2006Lawley et al, 2004;Boenigk et al, 2006;Bass et al, 2007;Caron, 2009). We would like to emphasize that all existing knowledge of microbial diversity comes from samples, and, strictly speaking, is limited to the collection of samples analyzed so far-rather than environments from which they were obtained.…”

The Proterozoic Record of Eukaryotes

“…Geographic isolation may also be responsible for the diversification of eukaryotic groups during the Cryogenian. Several recent studies have documented evidence of geographic isolation and divergence in modern protist groups (Boenigk et al 2006;Foissner et al 2007;Casteleyn et al 2010), suggesting that protists in modern ecosystems are not cosmopolitan. As such, global glaciation may have potentially stimulated diversification, while keeping overall abundance low.…”