We applied nucleic acid-based molecular methods, combined with estimates of biomass (ATP), pigments, and microelectrode measurements of chemical gradients, to map microbial diversity vertically on a millimeter scale in a hypersaline microbial mat from Guerrero Negro, Baja California Sur, Mexico. To identify the constituents of the mat, small-subunit rRNA genes were amplified by PCR from community genomic DNA extracted from layers, cloned, and sequenced. Bacteria dominated the mat and displayed unexpected and unprecedented diversity. The majority (1,336) of the 1,586 bacterial 16S rRNA sequences generated were unique, representing 752 species (>97% rRNA sequence identity) in 42 of the main bacterial phyla, including 15 novel candidate phyla. The diversity of the mat samples differentiated according to the chemical milieu defined by concentrations of O 2 and H 2 S. Bacteria of the phylum Chloroflexi formed the majority of the biomass by percentage of bulk rRNA and of clones in rRNA gene libraries. This result contradicts the general belief that cyanobacteria dominate these communities. Although cyanobacteria constituted a large fraction of the biomass in the upper few millimeters (>80% of the total rRNA and photosynthetic pigments), Chloroflexi sequences were conspicuous throughout the mat. Filamentous Chloroflexi bacteria were identified by fluorescence in situ hybridization within the polysaccharide sheaths of the prominent cyanobacterium Microcoleus chthonoplastes, in addition to free living in the mat. The biological complexity of the mat far exceeds that observed in other polysaccharide-rich microbial ecosystems, such as the human and mouse distal guts, and suggests that positive feedbacks exist between chemical complexity and biological diversity.
Mounting evidence indicates the presence of a near complete biological nitrogen cycle in redox-stratified oceans during the late Archean to early Proterozoic (c. 2.5-2.0 Ga). It has been suggested that the iron (Fe)- or vanadium (V)-dependent nitrogenase rather than molybdenum (Mo)-dependent form was responsible for dinitrogen fixation during this time because oceans were depleted in Mo and rich in Fe. We evaluated this hypothesis by examining the phylogenetic relationships of proteins that are required for the biosynthesis of the active site cofactor of Mo-nitrogenase in relation to structural proteins required for Fe-, V- and Mo-nitrogenase. The results are highly suggestive that among extant nitrogen-fixing organisms for which genomic information exists, Mo-nitrogenase is unlikely to have been associated with the Last Universal Common Ancestor. Rather, the origin of Mo-nitrogenase can be traced to an ancestor of the anaerobic and hydrogenotrophic methanogens with acquisition in the bacterial domain via lateral gene transfer involving an anaerobic member of the Firmicutes. A comparison of substitution rates estimated for proteins required for the biosynthesis of the nitrogenase active site cofactor and for a set of paralogous proteins required for the biosynthesis of bacteriochlorophyll suggests that Nif emerged from a nitrogenase-like ancestor approximately 1.5-2.2 Ga. An origin and ensuing proliferation of Mo-nitrogenase under anoxic conditions would likely have occurred in an environment where anaerobic methanogens and Firmicutes coexisted and where Mo was at least episodically available, such as in a redox-stratified Proterozoic ocean basin.
An understanding of how communities are organized is a fundamental goal of ecology but one which has historically been elusive for microbial systems. We used a bar-coded pyrosequencing approach targeting the V3 region of the bacterial small-subunit rRNA gene to address the factors that structure communities along the thermal gradients of two alkaline hot springs in the Lower Geyser Basin of Yellowstone National Park. The filtered data set included a total of nearly 34,000 sequences from 39 environmental samples. Each was assigned to one of 391 operational taxonomic units (OTUs) identified by their unique V3 sequence signatures. Although the two hot springs differed in their OTU compositions, community resemblance and diversity changed with strikingly similar dynamics along the two outflow channels. Two lines of evidence suggest that these community properties are controlled primarily by environmental temperature. First, community resemblance decayed exponentially with increasing differences in temperature between samples but was only weakly correlated with physical distance. Second, diversity decreased with increasing temperature at the same rate along both gradients but was uncorrelated with other measured environmental variables. This study also provides novel insights into the nature of the ecological interactions among important taxa in these communities. A strong negative association was observed between cyanobacteria and the Chloroflexi, which together accounted for ϳ70% of the sequences sampled. This pattern contradicts the longstanding hypothesis that coadapted lineages of these bacteria maintain tightly cooccurring distributions along these gradients as a result of a producerconsumer relationship. We propose that they instead compete for some limiting resource(s).Elucidating how biodiversity is distributed and the mechanisms underlying those patterns is a central goal of ecology. Although microorganisms make critical contributions to ecosystem function through their participation in biogeochemical cycles, we still have only a limited understanding of the factors that control the spatial structure and diversity of microbial communities (37). For example, although it is clear that microbial community composition is influenced by environmental variation (11,17,18,28), the question of how diversity changes along environmental gradients remains generally unresolved. Of particular interest is the relationship between microbial diversity and temperature, as this environmental variable is strongly correlated with diversity over a broad range of spatial scales for many plant and animal taxa in terrestrial, freshwater, and marine ecosystems (1,12,36,39,43). In addition, because spatially resolved abundance data for individual microbial taxa are scarce, we have only limited information regarding the patterns of association among microorganisms. Consequently, microbial ecology has developed with little clarity regarding the potential roles of either negative or positive biotic interactions for structuring communiti...
Chlorophyll d-producing cyanobacteria are a recently described group of phototrophic bacteria that is a major focus of photosynthesis research, previously known only from marine environments in symbiosis with eukaryotes. We have discovered a free-living member of this group from a eutrophic hypersaline lake. Phylogenetic analyses indicated these strains are closely related to each other but not to prochlorophyte cyanobacteria that also use an alternative form of chlorophyll as the major light-harvesting pigment. We have also demonstrated that these bacteria acquired a fragment of the small-subunit rRNA gene encoding a conserved hairpin in the bacterial ribosome from a proteobacterial donor at least 10 million years before the present. Thus, our most widely used phylogenetic marker can be a mosaic of sequence fragments with widely divergent evolutionary histories.cyanobacteria ͉ lateral gene transfer
The extension of ecological tolerance limits may be an important mechanism by which microorganisms adapt to novel environments, but it may come at the evolutionary cost of reduced performance under ancestral conditions. We combined a comparative physiological approach with phylogenetic analyses to study the evolution of thermotolerance in hot spring cyanobacteria of the genus Synechococcus. Among the 20 laboratory clones of Synechococcus isolated from collections made along an Oregon hot spring thermal gradient, four different 16S rRNA gene sequences were identified. Phylogenies constructed by using the sequence data indicated that the clones were polyphyletic but that three of the four sequence groups formed a clade. Differences in thermotolerance were observed for clones with different 16S rRNA gene sequences, and comparison of these physiological differences within a phylogenetic framework provided evidence that more thermotolerant lineages of Synechococcus evolved from less thermotolerant ancestors. The extension of the thermal limit in these bacteria was correlated with a reduction in the breadth of the temperature range for growth, which provides evidence that enhanced thermotolerance has come at the evolutionary cost of increased thermal specialization. This study illustrates the utility of using phylogenetic comparative methods to investigate how evolutionary processes have shaped historical patterns of ecological diversification in microorganisms.Has adaptation to novel environments by the extension of tolerance limits historically been an important mechanism by which the ecological requirements of microorganisms have diverged? While the breadth of physiological diversity exhibited by microorganisms suggests that this may be the case, the relevance of this mechanism is yet to be firmly established. Similarly, little is known about the consequences of this mode of adaptation for fitness in ancestral environments. For example, are there trade-offs or costs of adaptation such that there is a correlated loss in performance under ancestral conditions? Providing answers to the above questions may help microbiologists to better make sense of extant microbial diversity and its distribution on the planet.The cyanobacteria provide an excellent system for testing hypotheses concerning the evolution of tolerance. During its evolutionary history, this ancient lineage of oxygen-evolving, photoautotrophic bacteria has established itself in diverse aquatic and terrestrial habitats exhibiting wide ranges in temperature, salinity, water potential, pH, and irradiance (36). An example of ecological diversification in the cyanobacteria is the invasion of alkaline hot spring habitats across western North America, Asia, Africa, and possibly Europe by members of the genus Synechococcus (8). Hot spring outflows typically exhibit marked temperature gradients, and microbial communities containing Synechococcus generally develop in these systems at temperatures between ϳ45 and 73°C, the thermal maximum for photosynthetic life (3, ...
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