Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO2 concentrations

Probst, Alexander J.; Castelle, Cindy J.; Singh, Andrea; Brown, Christopher T.; Anantharaman, Karthik; Sharon, Itai; Hug, Laura A.; Burstein, David; Emerson, Joanne B.; Thomas, Brian C.; Banfield, Jillian F.

doi:10.1111/1462-2920.13362

Title: Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO₂ concentrations

Journal Article · Tue Apr 26 00:00:00 EDT 2016 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.13362· OSTI ID:1567074

Probst, Alexander J. ^[1]; Castelle, Cindy J. ^[1]; Singh, Andrea ^[1]; Brown, Christopher T. ^[1]; Anantharaman, Karthik ^[1]; Sharon, Itai ^[1]; Hug, Laura A. ^[1]; Burstein, David ^[1]; Emerson, Joanne B. ^[1]; Thomas, Brian C. ^[1]; Banfield, Jillian F. ^[2]

Univ. of California, Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

As in many deep underground environments, the microbial communities in subsurface high-CO₂ ecosystems remain relatively unexplored. Current research based on single-gene assays revealed a remarkable variety of organisms from little studied phyla in Crystal Geyser (Utah, USA), a site where deeply sourced CO₂-saturated fluids are erupted at the surface. To provide genomic resolution of the metabolisms of these organisms, we used a novel metagenomic approach to recover 227 high-quality genomes from 150 microbial species affiliated with 46 different phylum-level lineages. Bacteria from two novel phylum-level lineages have the capacity for CO₂ fixation. Analyses of carbon fixation pathways in all studied organisms revealed that the Wood-Ljungdahl pathway and the Calvin-Benson-Bassham Cycle occurred with the highest frequency, whereas the reverse TCA cycle was little used. We infer that this, and selection for form II RuBisCOs, are adaptions to high CO₂-concentrations. Yet, many autotrophs can also grow mixotrophically, a strategy that confers metabolic versatility. The assignment of 156 hydrogenases to 90 different organisms suggests that H₂ is an important inter-species energy currency even under gaseous CO₂-saturation. As a whole, metabolic analyses at the organism level provided insight into the biochemical cycles that support subsurface life under the extreme condition of CO₂ saturation.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1567074

Journal Information:: Environmental Microbiology, Vol. 19, Issue 2; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 115 works

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Exemplar Abstract for Wirthibacter wanneri Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/ex.38278	dataset	January 2020
Nomenclature Abstract for Wirthibacter wanneri Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38278	dataset	January 2020
Nomenclature Abstract for Wirthbacteria Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38402	dataset	January 2020
Nomenclature Abstract for Incertae sedis 620 Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38403	dataset	January 2020
Nomenclature Abstract for Incertae sedis 621 Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38404	dataset	January 2020
Nomenclature Abstract for Incertae sedis 622 Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/nm.38405	dataset	January 2020
Taxon Abstract for the Domain Archaea Woese, C. R. NamesforLife https://doi.org/10.1601/tx.1	dataset	January 1990
Taxon Abstract for the genus Wirthibacter Probst et al. 2017. Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38257	dataset	January 2020
Taxon Abstract for the species Wirthibacter wanneri Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38278	dataset	January 2020
Taxon Abstract for the class Incertae sedis 620 Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38403	dataset	January 2020
Taxon Abstract for the order Incertae sedis 621 Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38404	dataset	January 2020
Taxon Abstract for the family Incertae sedis 622 Probst et al. 2017 Parker, Charles Thomas; Garrity, George M. NamesforLife https://doi.org/10.1601/tx.38405	dataset	January 2020
Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface Probst, Alexander J.; Ladd, Bethany; Jarett, Jessica K. Nature Microbiology, Vol. 3, Issue 3 https://doi.org/10.1038/s41564-017-0098-y	journal	January 2018
Rice Paddy Nitrospirae Carry and Express Genes Related to Sulfate Respiration: Proposal of the New Genus “ Candidatus Sulfobium” Zecchin, Sarah; Mueller, Ralf C.; Seifert, Jana Applied and Environmental Microbiology, Vol. 84, Issue 5 https://doi.org/10.1128/aem.02224-17	journal	December 2017
Culture Independent Genomic Comparisons Reveal Environmental Adaptations for Altiarchaeales Bird, Jordan T.; Baker, Brett J.; Probst, Alexander J. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01221	journal	August 2016
Genomic Characteristics of Desulfonema ishimotonii Tokyo 01T Implying Horizontal Gene Transfer Among Phylogenetically Dispersed Filamentous Gliding Bacteria Watanabe, Miho; Kojima, Hisaya; Umezawa, Kazuhiro Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00227	journal	February 2019