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Title: Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle

Abstract

A critical step in the biogeochemical cycle of sulfur on Earth is microbial sulfate reduction, yet organisms from relatively few lineages have been implicated in this process. Previous studies using functional marker genes have detected abundant, novel dissimilatory sulfite reductases (DsrAB) that could confer the capacity for microbial sulfite/sulfate reduction but were not affiliated with known organisms. Thus, the identity of a significant fraction of sulfate/sulfite-reducing microbes has remained elusive. Here we report the discovery of the capacity for sulfate/sulfite reduction in the genomes of organisms from 13 bacterial and archaeal phyla, thereby more than doubling the number of microbial phyla associated with this process. Eight of the 13 newly identified groups are candidate phyla that lack isolated representatives, a finding only possible given genomes from metagenomes. Organisms from Verrucomicrobia and two candidate phyla, Candidatus Rokubacteria and Candidatus Hydrothermarchaeota, contain some of the earliest evolved dsrAB genes. The capacity for sulfite reduction has been laterally transferred in multiple events within some phyla, and a key gene potentially capable of modulating sulfur metabolism in associated cells has been acquired by putatively symbiotic bacteria. We conclude that current functional predictions based on phylogeny significantly underestimate the extent of sulfate/sulfite reduction across Earth'smore » ecosystems. Understanding the prevalence of this capacity is integral to interpreting the carbon cycle because sulfate reduction is often coupled to turnover of buried organic carbon. Our findings expand the diversity of microbial groups associated with sulfur transformations in the environment and motivate revision of biogeochemical process models based on microbial community composition.« less

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [5];  [6];  [7];  [8]; ORCiD logo [2];  [5]; ORCiD logo [9]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science, Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  2. Univ. of Vienna (Austria). Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry meets Microbiology
  3. Univ. of Southern California, Los Angeles, CA (United States). Center for Dark Energy Biosphere Investigations; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  5. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science, Berkeley, CA (United States)
  6. Univ. of Toronto, ON (Canada). Dept. of Civil Engineering
  7. Univ. of Hawaii, Manoa, Kaneohe, HI (United States). Hawaii Inst. of Marine Biology
  8. Leibniz Inst. DSMZ, Braunschweig (Germany). Dept. of Microorganisms, and German Collection of Microorganisms and Cell Cultures
  9. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science, Berkeley, CA (United States), and Dept. of Environmental Science, Policy, and Management; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1478346
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 12; Journal Issue: 7; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Anantharaman, Karthik, Hausmann, Bela, Jungbluth, Sean P., Kantor, Rose S., Lavy, Adi, Warren, Lesley A., Rappé, Michael S., Pester, Michael, Loy, Alexander, Thomas, Brian C., and Banfield, Jillian F. Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle. United States: N. p., 2018. Web. doi:10.1038/s41396-018-0078-0.
Anantharaman, Karthik, Hausmann, Bela, Jungbluth, Sean P., Kantor, Rose S., Lavy, Adi, Warren, Lesley A., Rappé, Michael S., Pester, Michael, Loy, Alexander, Thomas, Brian C., & Banfield, Jillian F. Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle. United States. doi:10.1038/s41396-018-0078-0.
Anantharaman, Karthik, Hausmann, Bela, Jungbluth, Sean P., Kantor, Rose S., Lavy, Adi, Warren, Lesley A., Rappé, Michael S., Pester, Michael, Loy, Alexander, Thomas, Brian C., and Banfield, Jillian F. Wed . "Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle". United States. doi:10.1038/s41396-018-0078-0. https://www.osti.gov/servlets/purl/1478346.
@article{osti_1478346,
title = {Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle},
author = {Anantharaman, Karthik and Hausmann, Bela and Jungbluth, Sean P. and Kantor, Rose S. and Lavy, Adi and Warren, Lesley A. and Rappé, Michael S. and Pester, Michael and Loy, Alexander and Thomas, Brian C. and Banfield, Jillian F.},
abstractNote = {A critical step in the biogeochemical cycle of sulfur on Earth is microbial sulfate reduction, yet organisms from relatively few lineages have been implicated in this process. Previous studies using functional marker genes have detected abundant, novel dissimilatory sulfite reductases (DsrAB) that could confer the capacity for microbial sulfite/sulfate reduction but were not affiliated with known organisms. Thus, the identity of a significant fraction of sulfate/sulfite-reducing microbes has remained elusive. Here we report the discovery of the capacity for sulfate/sulfite reduction in the genomes of organisms from 13 bacterial and archaeal phyla, thereby more than doubling the number of microbial phyla associated with this process. Eight of the 13 newly identified groups are candidate phyla that lack isolated representatives, a finding only possible given genomes from metagenomes. Organisms from Verrucomicrobia and two candidate phyla, Candidatus Rokubacteria and Candidatus Hydrothermarchaeota, contain some of the earliest evolved dsrAB genes. The capacity for sulfite reduction has been laterally transferred in multiple events within some phyla, and a key gene potentially capable of modulating sulfur metabolism in associated cells has been acquired by putatively symbiotic bacteria. We conclude that current functional predictions based on phylogeny significantly underestimate the extent of sulfate/sulfite reduction across Earth's ecosystems. Understanding the prevalence of this capacity is integral to interpreting the carbon cycle because sulfate reduction is often coupled to turnover of buried organic carbon. Our findings expand the diversity of microbial groups associated with sulfur transformations in the environment and motivate revision of biogeochemical process models based on microbial community composition.},
doi = {10.1038/s41396-018-0078-0},
journal = {The ISME Journal},
number = 7,
volume = 12,
place = {United States},
year = {2018},
month = {2}
}

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Cited by: 30 works
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