Evolution of Thermotolerance in Hot Spring Cyanobacteria of the GenusSynechococcus

Abstract

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, ...

Discovery of a free-living chlorophyll d -producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene

“…Sequences were aligned as described (10). Phylogenies were reconstructed from 1,412 nucleotides of SSU rRNA gene sequence data by maximum likelihood, parsimony, and neighbor-joining methods with PAUP*, Ver.…”

“…Protocols for genomic DNA isolation and thermal cycling were as described (10). The nearly complete 16S rRNA gene sequence was amplified as two fragments spanning E. coli positions 8-1334 and 359-1528 with primer sets AGAGTTTGATCMTGGCT-CAGG͞CTTCAYGYAGGCGAGTTGCAGC and GGGGA-AT YT TCCGCA ATGGG͞A A AGGAGGTGATCCAGCC.…”

Biophysical model of prokaryotic diversity in geothermal hot springs

“…They were able to measure temperature dependences of birth rates for their genetically distinct strains A, B, B', B'' and B'''; they were unable to cultivate their strain A', but noted it has similar characteristics to Group IV strains in Ref. 29 . In the one case (strain A') where data did not exist for the temperature dependence of the photosynthetic rate, we were able to use the same range, Given these field data results, we were able to use measured dependencies for birth rate and photosynthetic rate upon temperature wherever possible in our simulations (See Fig.…”

“…For example, none of the Oregon strains identified in Ref. 29 were identical to those found in Yellowstone National Park in Ref. 23 .…”

“…25 26 In particular, such methods have allowed the mapping of unexpectedly diverse lineages of thermophiles within hot springs environments. 14,24,[27][28][29][30] (In other work, high levels (97%) of similarity in 16S ribosomal RNA (rRNA) sequences can correspond to strains with very different environmental preferences, illustrating that such sequence similarity sets only a lower bound on diversity, as it does not rule out subpopulations with similar rRNA but different physiological properties. 19 ) Phylogenetic studies also have shown that community structure and species diversity in the hot spring systems considered here are determined primarily by water temperature, rather than chemical composition, pH or other factors.…”