Geographic Barriers Isolate Endemic Populations of Hyperthermophilic Archaea

Whitaker, Rachel J.; Grogan, Dennis W.; Taylor, John W.

doi:10.1126/science.1086909

Cited by 733 publications

(682 citation statements)

References 22 publications

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“…Within a narrow pH realm, the detection of dispersal limitation signifies not just that geographically proximal communities are more closely related phylogenetically but that local adaptation could be limited to isolated and persistent local communities, following the arguments of Hubbell (2001). These results are consistent with earlier examinations of species endemism in geothermal environments (Papke et al, 2003;Whitaker et al, 2003;Takacs-Vesbach et al, 2008) and show endemism of bacterial lineages at small spatial scales. In addition to the role of pH and GD, the results presented here allude to the importance of interspecies or interguild relationships (that is, phototrophs and fermentative bacteria) in structuring the genetic diversity of communities.…”

Section: Discussionsupporting

confidence: 81%

“…These findings are consistent with a number of recent studies focused on microbial communities ([ (Martiny et al, 2006) and references therein] (Whitaker et al, 2003)), which together challenge the long-held notion that 'everything is everywhere and the environment selects' and implicate the fundamental role of geographic constraints in the assembly of microbial lineages in natural communities. For example, an examination of endemic populations of the hyperthermophilic archaeon Sulfolobus using multi-locus sequence analysis revealed dispersal limitation in geothermal environments across large geographical scales spanning the Northern hemisphere (Whitaker et al, 2003). Similarly, Papke et al (Papke et al, 2003), showed geographic isolation in cyanobacterial populations sampled from geothermal springs from geographically distinct environments across the globe.…”

Section: Discussionsupporting

confidence: 81%

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[FeFe]-hydrogenase in Yellowstone National Park: evidence for dispersal limitation and phylogenetic niche conservatism

et al. 2010

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Hydrogen (H 2 ) has an important role in the anaerobic degradation of organic carbon and is the basis for many syntrophic interactions that commonly occur in microbial communities. Little is known, however, with regard to the biotic and/or abiotic factors that control the distribution and phylogenetic diversity of organisms which produce H 2 in microbial communities. In this study, we examined the [FeFe]-hydrogenase gene (hydA) as a proxy for fermentative bacterial H 2 production along physical and chemical gradients in various geothermal springs in Yellowstone National Park (YNP), WY, USA. The distribution of hydA in YNP geothermal springs was constrained by pH to environments co-inhabited by oxygenic phototrophs and to environments predicted to have low inputs of abiotic H 2 . The individual HydA asssemblages from YNP springs were more closely related when compared with randomly assembled communities, which suggests ecological filtering. Model selection approaches revealed that geographic distance was the best explanatory variable to predict the phylogenetic relatedness of HydA communities. This evinces the dispersal limitation imposed by the geothermal spring environment on HydA phylogenetic diversity even at small spatial scales. pH differences between sites is the second highest ranked explanatory variable of HydA phylogenetic relatedness, which suggests that the ecology related to pH imposes strong phylogenetic niche conservatism. Collectively, these results indicate that pH has imposed strong niche conservatism on fermentative bacteria and that, within a narrow pH realm, YNP springs are dispersal limited with respect to fermentative bacterial communities.

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Section: Discussionsupporting

confidence: 81%

Section: Discussionsupporting

confidence: 81%

[FeFe]-hydrogenase in Yellowstone National Park: evidence for dispersal limitation and phylogenetic niche conservatism

et al. 2010

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“…Deep-sea currents provide a plausible mechanism for the mixing of Arctic and Antarctic psychrophilic communities. Alternatively, this community similarity could be a result of the current level of resolution in the available molecular data, as suggested by Whitaker et al (55). In-depth comparisons between the genomes of psychrophiles from the two hemispheres, along with those of related piezophiles, should be undertaken to better evaluate this hypothesis.…”

Section: Resultsmentioning

confidence: 99%

The Unique 16S rRNA Genes of Piezophiles Reflect both Phylogeny and Adaptation

Lauro

Chastain

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et al. 2007

Appl Environ Microbiol

124

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In the ocean's most extreme depths, pressures of 70 to 110 megapascals prevent the growth of all but the most hyperpiezophilic (pressure-loving) organisms. The physiological adaptations required for growth under these conditions are considered to be substantial. Efforts to determine specific adaptations permitting growth at extreme pressures have thus far focused on relatively few ␥-proteobacteria, in part due to the technical difficulties of obtaining piezophilic bacteria in pure culture. Here, we present the molecular phylogenies of several new piezophiles of widely differing geographic origins. Included are results from an analysis of the first deep-trench bacterial isolates recovered from the southern hemisphere (9.9-km depth) and of the first grampositive piezophilic strains. These new data allowed both phylogenetic and structural 16S rRNA comparisons among deep-ocean trench piezophiles and closely related strains not adapted to high pressure. Our results suggest that (i) the Circumpolar Deep Water acts as repository for hyperpiezophiles and drives their dissemination to deep trenches in the Pacific Ocean and (ii) the occurrence of elongated helices in the 16S rRNA genes increases with the extent of adaptation to growth at elevated pressure. These helix changes are believed to improve ribosome function under deep-sea conditions. Low temperature and high hydrostatic pressure structure deep-sea communities outside of hydrothermal vents. Tight selection by these and other environmental parameters is considered the cause of the conspicuous absence of many deep-sea taxonomic groups from the deepest ocean environments (8, 44).Both temperature and pressure exert their effects at many levels of bacterial physiology, from the structure of macromolecules to the rate of metabolic reactions. Adaptations to low temperature include alterations of membrane phospholipids, such as increased fatty acid unsaturation (43), enzymes characterized by high catalytic efficiency and reduced activation enthalpy (16,20,37,45), and high levels of cold shock proteins, RNA helicases (9), and posttranscriptional modification of tRNA molecules (15), all of which may reduce the formation of unfavorable nucleic acid secondary structures at low temperature. In contrast with enthalpy-based temperature effects, the underlying cause of pressure effects arises from the promotion of reduced system volumes, in accordance with Le Chatelier's principle (5). Despite these thermodynamic differences, low temperature and high pressure share a surprising number of influences on biological processes. For example, membrane fluidity, permeability, and phase are similarly altered by both parameters.As with psychrophiles, piezophiles ("high-pressure-loving" microbes) contain lipids with highly unsaturated fatty acids (6, 7). Indeed, the presence of unsaturated fatty acids is critical to growth ability at high pressure (3,4,19). Both low temperature and high pressure also alter protein quaternary structure (46) and nucleic acid secondary structure (50), and at ...

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“…Microbial biography studies in hot springs, a great number carried out in Yellowstone National Park, have shown these environments containing highly distinct community structures, where archaea, cyanobacteria, chloroflexi and acidobacteria are among the microorganisms most commonly found [35,40,[50][51]23,56]. Such studies have typically focused on the broader microbial community and very little is known on the biogeography of actinobacteria in hot springs.…”

Section: Introductionmentioning

confidence: 99%