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Title: SAR11 bacteria linked to ocean anoxia and nitrogen loss

Abstract

Bacteria of the SAR11 clade constitute up to one half of all microbial cells in the oxygen-rich surface ocean. SAR11 bacteria are also abundant in oxygen minimum zones (OMZs), where oxygen falls below detection and anaerobic microbes have vital roles in converting bioavailable nitrogen to N 2 gas. Anaerobic metabolism has not yet been observed in SAR11, and it remains unknown how these bacteria contribute to OMZ biogeochemical cycling. Here in this paper, genomic analysis of single cells from the world's largest OMZ revealed previously uncharacterized SAR11 lineages with adaptations for life without oxygen, including genes for respiratory nitrate reductases (Nar). SAR11 nar genes were experimentally verified to encode proteins catalysing the nitrite-producing first step of denitrification and constituted ~40% of OMZ nar transcripts, with transcription peaking in the anoxic zone of maximum nitrate reduction activity. Finally, these results link SAR11 to pathways of ocean nitrogen loss, redefining the ecological niche of Earth's most abundant organismal group.

Authors:
 [1];  [2];  [3];  [3];  [2];  [2];  [2];  [2];  [3];  [2];  [4];  [5];  [6];  [7];  [6];  [3];  [8];  [2]
  1. Georgia Institute of Technology, Atlanta, GA (United States). School of Civil and Environmental Engineering
  2. Georgia Institute of Technology, Atlanta, GA (United States). School of Biological Sciences
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Bowdoin College, Brunswick, ME (United States). Dept. of Biology
  5. Max Planck Institute for Marine Microbiology (Germany). Biochemistry Group
  6. University of Southern Denmark (Denmark). Department of Biology and Nordic Center for Earth Evolution (NordCEE)
  7. Georgia Institute of Technology, Atlanta, GA (United States). School of Earth and Atmospheric Sciences
  8. Georgia Institute of Technology, Atlanta, GA (United States). School of Civil and Environmental Engineering and School of Biological 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:
1379554
Grant/Contract Number:
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 536; Journal Issue: 7615; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Water microbiology; Element cycles; Marine biology

Citation Formats

Tsementzi, Despina, Wu, Jieying, Deutsch, Samuel, Nath, Sangeeta, Rodriguez-R, Luis M., Burns, Andrew S., Ranjan, Piyush, Sarode, Neha, Malmstrom, Rex R., Padilla, Cory C., Stone, Benjamin K., Bristow, Laura A., Larsen, Morten, Glass, Jennifer B., Thamdrup, Bo, Woyke, Tanja, Konstantinidis, Konstantinos T., and Stewart, Frank J. SAR11 bacteria linked to ocean anoxia and nitrogen loss. United States: N. p., 2016. Web. doi:10.1038/nature19068.
Tsementzi, Despina, Wu, Jieying, Deutsch, Samuel, Nath, Sangeeta, Rodriguez-R, Luis M., Burns, Andrew S., Ranjan, Piyush, Sarode, Neha, Malmstrom, Rex R., Padilla, Cory C., Stone, Benjamin K., Bristow, Laura A., Larsen, Morten, Glass, Jennifer B., Thamdrup, Bo, Woyke, Tanja, Konstantinidis, Konstantinos T., & Stewart, Frank J. SAR11 bacteria linked to ocean anoxia and nitrogen loss. United States. doi:10.1038/nature19068.
Tsementzi, Despina, Wu, Jieying, Deutsch, Samuel, Nath, Sangeeta, Rodriguez-R, Luis M., Burns, Andrew S., Ranjan, Piyush, Sarode, Neha, Malmstrom, Rex R., Padilla, Cory C., Stone, Benjamin K., Bristow, Laura A., Larsen, Morten, Glass, Jennifer B., Thamdrup, Bo, Woyke, Tanja, Konstantinidis, Konstantinos T., and Stewart, Frank J. 2016. "SAR11 bacteria linked to ocean anoxia and nitrogen loss". United States. doi:10.1038/nature19068. https://www.osti.gov/servlets/purl/1379554.
@article{osti_1379554,
title = {SAR11 bacteria linked to ocean anoxia and nitrogen loss},
author = {Tsementzi, Despina and Wu, Jieying and Deutsch, Samuel and Nath, Sangeeta and Rodriguez-R, Luis M. and Burns, Andrew S. and Ranjan, Piyush and Sarode, Neha and Malmstrom, Rex R. and Padilla, Cory C. and Stone, Benjamin K. and Bristow, Laura A. and Larsen, Morten and Glass, Jennifer B. and Thamdrup, Bo and Woyke, Tanja and Konstantinidis, Konstantinos T. and Stewart, Frank J.},
abstractNote = {Bacteria of the SAR11 clade constitute up to one half of all microbial cells in the oxygen-rich surface ocean. SAR11 bacteria are also abundant in oxygen minimum zones (OMZs), where oxygen falls below detection and anaerobic microbes have vital roles in converting bioavailable nitrogen to N2 gas. Anaerobic metabolism has not yet been observed in SAR11, and it remains unknown how these bacteria contribute to OMZ biogeochemical cycling. Here in this paper, genomic analysis of single cells from the world's largest OMZ revealed previously uncharacterized SAR11 lineages with adaptations for life without oxygen, including genes for respiratory nitrate reductases (Nar). SAR11 nar genes were experimentally verified to encode proteins catalysing the nitrite-producing first step of denitrification and constituted ~40% of OMZ nar transcripts, with transcription peaking in the anoxic zone of maximum nitrate reduction activity. Finally, these results link SAR11 to pathways of ocean nitrogen loss, redefining the ecological niche of Earth's most abundant organismal group.},
doi = {10.1038/nature19068},
journal = {Nature (London)},
number = 7615,
volume = 536,
place = {United States},
year = 2016,
month = 8
}

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  • Small-subunit (SSU) ribosomal DNA (rDNA) gene clusters are phylogenetically related sets of SSU rRNA genes, commonly encountered in genes amplified from natural populations. Genetic variability in gene clusters could result form artifacts (polymerase error or PCR chimera formation), microevolution (variation among rrn copies within strains), or macroevolution (genetic divergence correlated with long-term evolutionary divergence). To better understand gene clusters, this study assessed genetic diversity and distribution of a single environmental SSU rDNA gene cluster, the SAR11 cluster. SAR11 cluster genes, from an uncultured group of the {alpha} subclass of the class Proteobacteria, have been recovered from coastal and midoceanic watersmore » of the North Atlantic and Pacific. We cloned and bidirectionally sequenced 23 new SAR11 cluster 16S rRNA genes, from 80 and 250 m im the Sargasso Sea and from surface coastal waters of the Atlantic and Pacific, and analyzed them with previously published sequences. Two SAR11 genes were obviously PCR chimeras, but the biological (nonchimeric) origins of most subgroups within the cluster were confirmed by independent recovery from separate gene libraries. Using group-specific oligonucleotide probes, we analyzed depth profiles of nucleic acids, targeting both amplified rDNAs and bulk RNAs. Two subgroups within the SAR11 cluster showed different highly depth-specific distributions. We conclude that some of the genetic diversity within the SAR11 gene cluster represents macroevolutionary divergence correlated with niche specialization. Furthermore, we demonstrate the utility for marine microbial ecology of oligonucleotide probes based on gene sequences amplified from natural populations and show that a detailed knowledge of sequence variability may be needed to effectively design these probes. 48 refs., 7 figs., 3 tabs.« less
  • The distribution and abundance of sulfate-reducing bacteria (SRB) and eukaryotes within the upper 4 mm of a hypersaline cyanobacterial mat community were characterized at high resolution with group-specific hybridization probes to quantify 16S rRNA extracted from 100-{micro}m depth intervals. This revealed a preferential localization of SRB within the region defined by the oxygen chemocline. Among the different groups of SRB quantified, including members of the provisional families Desulfovibrionaceae and Desulfobacteriaceae, Desulfonema-like populations dominated and accounted for up to 30% of total rRNA extracted from certain depth intervals of the chemocline. These data suggest that recognized genera of SRB are notmore » necessarily restricted by high levels of oxygen in this mat community and the possibility of significant sulfur cycling within the chemocline. In marked contrast, eukaryotic populations in this community demonstrated a preference for regions of anoxia.« less
  • Shigella sonnei cells were exposed to nitric oxide of Nethylmaleimide, the sulphydryl content of the treated bacteria was determined, and the bacteria were irradiated with x rays. The nitric oxide or N-ethylmaleimide treatment was found to decrease the sulphydryl content and the protective effect of anoxia against radiation in the bacteria cells. Cysteine was found to increase the protective effect of anoxia slightly for untreated cells. Reasons are given for believing the decrease in axonic protection to be due to the reduction of the intracellular sulphydryl compounds. (D.L.C.)