Dataset Information

Temperature impacts community structure and function of phototrophic Chloroflexi and Cyanobacteria in two alkaline hot springs in Yellowstone National Park.

ABSTRACT: Photosynthetic bacteria are abundant in alkaline, terrestrial hot springs and there is a long history of research on phototrophs in Yellowstone National Park (YNP). Hot springs provide a framework to examine the ecophysiology of phototrophs in situ because they provide natural gradients of geochemistry, pH and temperature. Phototrophs within the Cyanobacteria and Chloroflexi groups are frequently observed in alkaline hot springs. Decades of research has determined that temperature constrains Cyanobacteria in alkaline hot springs, but factors that constrain the distribution of phototrophic Chloroflexi remain unresolved. Using a combination of 16S rRNA gene sequencing and photoassimilation microcosms, we tested the hypothesis that temperature would constrain the activity and composition of phototrophic Cyanobacteria and Chloroflexi. We expected diversity and rates of photoassimilation to decrease with increasing temperature. We report 16S rRNA amplicon sequencing along with carbon isotope signatures and photoassimilation from 45 to 72°C in two alkaline hot springs. We find that Roseiflexus, Chloroflexus (Chloroflexi) and Leptococcus (Cyanobacteria) operational taxonomic units (OTUs) have distinct distributions with temperature. This distribution suggests that, like phototrophic Cyanobacteria, temperature selects for specific phototrophic Chloroflexi taxa. The richness of phototrophic Cyanobacteria decreased with increasing temperature along with a decrease in oxygenic photosynthesis, whereas Chloroflexi richness and rates of anoxygenic photosynthesis did not decrease with increasing temperature, even at temperatures approaching the upper limit of photosynthesis (~72-73°C). Our carbon isotopic data suggest an increasing prevalence of the 3-hydroxypropionate pathway with decreasing temperature coincident with photoautotrophic Chloroflexi. Together these results indicate temperature plays a role in defining the niche space of phototrophic Chloroflexi (as has been observed for Cyanobacteria), but other factors such as morphology, geochemistry, or metabolic diversity of Chloroflexi, in addition to temperature, could determine the niche space of this highly versatile group.

SUBMITTER: Bennett AC

PROVIDER: S-EPMC7540483 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Temperature impacts community structure and function of phototrophic Chloroflexi and Cyanobacteria in two alkaline hot springs in Yellowstone National Park.

Bennett Annastacia C AC Murugapiran Senthil K SK Hamilton Trinity L TL

Environmental microbiology reports 20200726 5

Photosynthetic bacteria are abundant in alkaline, terrestrial hot springs and there is a long history of research on phototrophs in Yellowstone National Park (YNP). Hot springs provide a framework to examine the ecophysiology of phototrophs in situ because they provide natural gradients of geochemistry, pH and temperature. Phototrophs within the Cyanobacteria and Chloroflexi groups are frequently observed in alkaline hot springs. Decades of research has determined that temperature constrains Cya ...[more]

PMID: 32613733

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Project description:Alkaline hot springs in Yellowstone National Park (YNP) provide a framework to study the relationship between photoautotrophs and temperature. Previous work has focused on studying how cyanobacteria (oxygenic phototrophs) vary with temperature, sulfide, and pH, but many questions remain regarding the ecophysiology of anoxygenic photosynthesis due to the taxonomic and metabolic diversity of these taxa. To this end, we examined the distribution of genes involved in phototrophy, carbon fixation, and nitrogen fixation in eight alkaline (pH 7.3-9.4) hot spring sites near the upper temperature limit of photosynthesis (71ºC) in YNP using metagenome sequencing. Based on genes encoding key reaction center proteins, geographic isolation plays a larger role than temperature in selecting for distinct phototrophic Chloroflexi, while genes typically associated with autotrophy in anoxygenic phototrophs, did not have distinct distributions with temperature. Additionally, we recovered Calvin cycle gene variants associated with Chloroflexi, an alternative carbon fixation pathway in anoxygenic photoautotrophs. Lastly, we recovered several abundant nitrogen fixation gene sequences associated with Roseiflexus, providing further evidence that genes involved in nitrogen fixation in Chloroflexi are more common than previously assumed. Together, our results add to the body of work on the distribution and functional potential of phototrophic bacteria in Yellowstone National Park hot springs and support the hypothesis that a combination of abiotic and biotic factors impact the distribution of phototrophic bacteria in hot springs. Future studies of isolates and metagenome assembled genomes (MAGs) from these data and others will further our understanding of the ecology and evolution of hot spring anoxygenic phototrophs. IMPORTANCE Photosynthetic bacteria in hot springs are of great importance to both microbial evolution and ecology. While a large body of work has focused on oxygenic photosynthesis in cyanobacteria in Mushroom and Octopus Springs in Yellowstone National Park, many questions remain regarding the metabolic potential and ecology of hot spring anoxygenic phototrophs. Anoxygenic phototrophs are metabolically and taxonomically diverse, and further investigations into their physiology will lead to a deeper understanding of microbial evolution and ecology of these taxa. Here, we have quantified the distribution of key genes involved in carbon and nitrogen metabolism in both oxygenic and anoxygenic phototrophs. Our results suggest that temperature >68ºC selects for distinct groups of cyanobacteria and that carbon fixation pathways associated with these taxa are likely subject to the same selective pressure. Additionally, our data suggest that phototrophic Chloroflexi genes and carbon fixation genes are largely influenced by local conditions as evidenced by our gene variant analysis. Lastly, we recovered several genes associated with potentially novel phototrophic Chloroflexi. Together, our results add to the body of work on hot springs in Yellowstone National Park and set the stage for future work on metagenome assembled genomes.

Project description:Geographic isolation can be a main driver of microbial evolution in hot springs while temperature plays a role on local scales. For example, cyanobacteria, particularly high-temperature Synechococcus spp., have undergone ecological diversification along temperature gradients in hot spring outflow channels. While water flow, and thus temperature, is largely stable in many hot springs, flow can vary in geysing/eruptive hot springs, resulting in large temperature fluctuations (sometimes more than 40°C). However, the role of large temperature fluctuations in driving diversification of cyanobacteria in eruptive hot springs has not been explored. Here, we examined phototroph community composition and potential photoautotrophic activity in two alkaline eruptive hot springs with similar geochemistry in the Lower Geyser Basin in Yellowstone National Park, WY. We observed distinct cyanobacterial amplicon sequencing variants (ASVs) consistent with allopatry and levels of light-dependent inorganic carbon uptake rates similar to other hot springs, despite large temperature fluctuations. Our data suggest median temperatures may drive phototroph fitness in eruptive hot springs while future studies are necessary to determine the evolutionary consequences of thriving under continuously fluctuating temperatures. We propose that large temperature swings in eruptive hot springs offer unique environments to examine the role of allopatry versus physical and chemical characteristics of ecosystems in driving cyanobacterium evolution and add to the debate regarding the ecology of thermal adaptation and the potential for narrowing niche breadth with increasing temperature. IMPORTANCE Hot spring cyanobacteria have long been model systems for examining ecological diversification as well as characterizing microbial adaptation and evolution to extreme environments. These studies have reported cyanobacterial diversification in hot spring outflow channels that can be defined by distinct temperature ranges. Our study builds on these previous studies by examining cyanobacteria in geysing hot springs. Geysing hot springs result in outflow channels that experience regular and large temperature fluctuations. While community compositions are similar between geysing and nongeysing hot spring outflow channels, our data suggest median, rather than high, temperature drives the fitness of cyanobacteria in geysing hot springs. We propose that large temperature swings may result in patterns of ecological diversification that are distinct from more stable outflows.

Dataset Information

Temperature impacts community structure and function of phototrophic Chloroflexi and Cyanobacteria in two alkaline hot springs in Yellowstone National Park.

Publications

Temperature impacts community structure and function of phototrophic Chloroflexi and Cyanobacteria in two alkaline hot springs in Yellowstone National Park.

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