Temperature and Geographic Location Impact the Distribution and Diversity of Photoautotrophic Gene Variants in Alkaline Yellowstone Hot Springs

Annastacia C. Bennett; Senthil Murugapiran; Eric D. Kees; Hailey M. Sauer; Trinity L. Hamilton

doi:10.1128/spectrum.01465-21

Temperature and Geographic Location Impact the Distribution and Diversity of Photoautotrophic Gene Variants in Alkaline Yellowstone Hot Springs

Annastacia C. Bennett, Senthil Murugapiran, Eric D. Kees, Hailey M. Sauer, Trinity L. Hamilton

Plant and Microbial Biology

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

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 (718C) 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 .688C 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.

Original language	English (US)
Journal	Microbiology Spectrum
Volume	10
Issue number	3
DOIs	https://doi.org/10.1128/spectrum.01465-21
State	Published - Jun 2022

Bibliographical note

Funding Information:
We first acknowledge that Yellowstone National Park was established on the traditional and sacred land of 27 tribes who hunted, fished, gathered, and conducted religious ceremonies using the thermal waters and land in Yellowstone. This land acknowledgment is an intentional act to counter the erasure of Indigenous Peoples and to demonstrate respect for their sovereign rights. We are grateful to the entire staff of the Yellowstone Research Permit Office for facilitating the permitting process to perform research in YNP. T.L.H. conducts research in Yellowstone National Park under research permit YELL-2018-SCI-7020 issued by the Yellowstone Research Permit Office and reviewed annually. This work was supported by the University of Minnesota. T.L.H., A.C.B., E.D.K., and S.K.M. were supported by NASA Exobiology award number 80NSSC20K0614. The authors acknowledge the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper. Special thanks to Annie Carlson and Erik Oberg in the Yellowstone Research Permit Office. We thank J. Havig, L. Brengman, C. Grettenberger, L. Seyler, and J. Kuether for technical assistance in the field and A. Borowski and K. Quinn for assistance processing samples in the lab. A.C.B and T.L.H. designed the study and completed the laboratory analyses. A.C.B. and T.L.H. collected samples and performed the field and lab work. A.C.B., S.K.M., E.D.K., H.M.S., and T.L.H. analyzed the data. A.C.B interpreted the data and wrote the manuscript with contributions from S.K.M., E.D.K., H.M.S., and T.L.H. We declare no competing financial interests.

Funding Information:
We first acknowledge that Yellowstone National Park was established on the traditional and sacred land of 27 tribes who hunted, fished, gathered, and conducted religious ceremonies using the thermal waters and land in Yellowstone. This land acknowledgment is an intentional act to counter the erasure of Indigenous Peoples and to demonstrate respect for their sovereign rights. We are grateful to the entire staff of the Yellowstone Research Permit Office for facilitating the permitting process to perform research in YNP. T.L.H. conducts research in Yellowstone National Park under research permit YELL-2018-SCI-7020 issued by the Yellowstone Research Permit Office and reviewed annually. This work was supported by the University of Minnesota. T.L.H., A.C.B., E.D.K., and S.K.M. were supported by NASA Exobiology award number 80NSSC20K0614.

Publisher Copyright:
Copyright © 2022 Bennett et al.

Keywords

Chloroflexi
anoxygenic photosynthesis
cyanobacteria
hot springs
metagenomics
photosynthesis
phototroph

PubMed: MeSH publication types

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't

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10.1128/spectrum.01465-21

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@article{fca7c64f1860438a8344f05a9b71127d,

title = "Temperature and Geographic Location Impact the Distribution and Diversity of Photoautotrophic Gene Variants in Alkaline Yellowstone Hot Springs",

abstract = "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 (718C) 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 .688C 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.",

keywords = "Chloroflexi, anoxygenic photosynthesis, cyanobacteria, hot springs, metagenomics, photosynthesis, phototroph",

author = "Bennett, {Annastacia C.} and Senthil Murugapiran and Kees, {Eric D.} and Sauer, {Hailey M.} and Hamilton, {Trinity L.}",

note = "Funding Information: We first acknowledge that Yellowstone National Park was established on the traditional and sacred land of 27 tribes who hunted, fished, gathered, and conducted religious ceremonies using the thermal waters and land in Yellowstone. This land acknowledgment is an intentional act to counter the erasure of Indigenous Peoples and to demonstrate respect for their sovereign rights. We are grateful to the entire staff of the Yellowstone Research Permit Office for facilitating the permitting process to perform research in YNP. T.L.H. conducts research in Yellowstone National Park under research permit YELL-2018-SCI-7020 issued by the Yellowstone Research Permit Office and reviewed annually. This work was supported by the University of Minnesota. T.L.H., A.C.B., E.D.K., and S.K.M. were supported by NASA Exobiology award number 80NSSC20K0614. The authors acknowledge the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper. Special thanks to Annie Carlson and Erik Oberg in the Yellowstone Research Permit Office. We thank J. Havig, L. Brengman, C. Grettenberger, L. Seyler, and J. Kuether for technical assistance in the field and A. Borowski and K. Quinn for assistance processing samples in the lab. A.C.B and T.L.H. designed the study and completed the laboratory analyses. A.C.B. and T.L.H. collected samples and performed the field and lab work. A.C.B., S.K.M., E.D.K., H.M.S., and T.L.H. analyzed the data. A.C.B interpreted the data and wrote the manuscript with contributions from S.K.M., E.D.K., H.M.S., and T.L.H. We declare no competing financial interests. Funding Information: We first acknowledge that Yellowstone National Park was established on the traditional and sacred land of 27 tribes who hunted, fished, gathered, and conducted religious ceremonies using the thermal waters and land in Yellowstone. This land acknowledgment is an intentional act to counter the erasure of Indigenous Peoples and to demonstrate respect for their sovereign rights. We are grateful to the entire staff of the Yellowstone Research Permit Office for facilitating the permitting process to perform research in YNP. T.L.H. conducts research in Yellowstone National Park under research permit YELL-2018-SCI-7020 issued by the Yellowstone Research Permit Office and reviewed annually. This work was supported by the University of Minnesota. T.L.H., A.C.B., E.D.K., and S.K.M. were supported by NASA Exobiology award number 80NSSC20K0614. Publisher Copyright: Copyright {\textcopyright} 2022 Bennett et al.",

year = "2022",

month = jun,

doi = "10.1128/spectrum.01465-21",

language = "English (US)",

volume = "10",

journal = "Microbiology Spectrum",

issn = "2165-0497",

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T1 - Temperature and Geographic Location Impact the Distribution and Diversity of Photoautotrophic Gene Variants in Alkaline Yellowstone Hot Springs

AU - Bennett, Annastacia C.

AU - Murugapiran, Senthil

AU - Kees, Eric D.

AU - Sauer, Hailey M.

AU - Hamilton, Trinity L.

N1 - Funding Information: We first acknowledge that Yellowstone National Park was established on the traditional and sacred land of 27 tribes who hunted, fished, gathered, and conducted religious ceremonies using the thermal waters and land in Yellowstone. This land acknowledgment is an intentional act to counter the erasure of Indigenous Peoples and to demonstrate respect for their sovereign rights. We are grateful to the entire staff of the Yellowstone Research Permit Office for facilitating the permitting process to perform research in YNP. T.L.H. conducts research in Yellowstone National Park under research permit YELL-2018-SCI-7020 issued by the Yellowstone Research Permit Office and reviewed annually. This work was supported by the University of Minnesota. T.L.H., A.C.B., E.D.K., and S.K.M. were supported by NASA Exobiology award number 80NSSC20K0614. The authors acknowledge the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper. Special thanks to Annie Carlson and Erik Oberg in the Yellowstone Research Permit Office. We thank J. Havig, L. Brengman, C. Grettenberger, L. Seyler, and J. Kuether for technical assistance in the field and A. Borowski and K. Quinn for assistance processing samples in the lab. A.C.B and T.L.H. designed the study and completed the laboratory analyses. A.C.B. and T.L.H. collected samples and performed the field and lab work. A.C.B., S.K.M., E.D.K., H.M.S., and T.L.H. analyzed the data. A.C.B interpreted the data and wrote the manuscript with contributions from S.K.M., E.D.K., H.M.S., and T.L.H. We declare no competing financial interests. Funding Information: We first acknowledge that Yellowstone National Park was established on the traditional and sacred land of 27 tribes who hunted, fished, gathered, and conducted religious ceremonies using the thermal waters and land in Yellowstone. This land acknowledgment is an intentional act to counter the erasure of Indigenous Peoples and to demonstrate respect for their sovereign rights. We are grateful to the entire staff of the Yellowstone Research Permit Office for facilitating the permitting process to perform research in YNP. T.L.H. conducts research in Yellowstone National Park under research permit YELL-2018-SCI-7020 issued by the Yellowstone Research Permit Office and reviewed annually. This work was supported by the University of Minnesota. T.L.H., A.C.B., E.D.K., and S.K.M. were supported by NASA Exobiology award number 80NSSC20K0614. Publisher Copyright: Copyright © 2022 Bennett et al.

PY - 2022/6

Y1 - 2022/6

N2 - 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 (718C) 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 .688C 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.

AB - 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 (718C) 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 .688C 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.

KW - Chloroflexi

KW - anoxygenic photosynthesis

KW - cyanobacteria

KW - hot springs

KW - metagenomics

KW - photosynthesis

KW - phototroph

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Temperature and Geographic Location Impact the Distribution and Diversity of Photoautotrophic Gene Variants in Alkaline Yellowstone Hot Springs

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