Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics

Kristin Bergauer, Antonio Fernandez-Guerra, Juan A L Garcia, Richard R Sprenger, Ramunas Stepanauskas, Maria G Pachiadaki, Ole N Jensen, Gerhard J Herndl

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Resumé

The phylogenetic composition of the heterotrophic microbial community is depth stratified in the oceanic water column down to abyssopelagic layers. In the layers below the euphotic zone, it has been suggested that heterotrophic microbes rely largely on solubilized particulate organic matter as a carbon and energy source rather than on dissolved organic matter. To decipher whether changes in the phylogenetic composition with depth are reflected in changes in the bacterial and archaeal transporter proteins, we generated an extensive metaproteomic and metagenomic dataset of microbial communities collected from 100- to 5,000-m depth in the Atlantic Ocean. By identifying which compounds of the organic matter pool are absorbed, transported, and incorporated into microbial cells, intriguing insights into organic matter transformation in the deep ocean emerged. On average, solute transporters accounted for 23% of identified protein sequences in the lower euphotic and ∼39% in the bathypelagic layer, indicating the central role of heterotrophy in the dark ocean. In the bathypelagic layer, substrate affinities of expressed transporters suggest that, in addition to amino acids, peptides and carbohydrates, carboxylic acids and compatible solutes may be essential substrates for the microbial community. Key players with highest expression of solute transporters were Alphaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria, accounting for 40%, 11%, and 10%, respectively, of relative protein abundances. The in situ expression of solute transporters indicates that the heterotrophic prokaryotic community is geared toward the utilization of similar organic compounds throughout the water column, with yet higher abundances of transporters targeting aromatic compounds in the bathypelagic realm.

OriginalsprogEngelsk
TidsskriftProceedings of the National Academy of Sciences of the United States of America
Vol/bind115
Udgave nummer3
Sider (fra-til)E400-E408
ISSN0027-8424
DOI
StatusUdgivet - 16. jan. 2018

Fingeraftryk

Archaeal Proteins
Heterotrophic Processes
Metagenomics
Particulate Matter
Proteins
Amino Acids
Peptides
Datasets

Citer dette

Bergauer, Kristin ; Fernandez-Guerra, Antonio ; Garcia, Juan A L ; Sprenger, Richard R ; Stepanauskas, Ramunas ; Pachiadaki, Maria G ; Jensen, Ole N ; Herndl, Gerhard J. / Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. I: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Bind 115, Nr. 3. s. E400-E408.
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title = "Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics",
abstract = "The phylogenetic composition of the heterotrophic microbial community is depth stratified in the oceanic water column down to abyssopelagic layers. In the layers below the euphotic zone, it has been suggested that heterotrophic microbes rely largely on solubilized particulate organic matter as a carbon and energy source rather than on dissolved organic matter. To decipher whether changes in the phylogenetic composition with depth are reflected in changes in the bacterial and archaeal transporter proteins, we generated an extensive metaproteomic and metagenomic dataset of microbial communities collected from 100- to 5,000-m depth in the Atlantic Ocean. By identifying which compounds of the organic matter pool are absorbed, transported, and incorporated into microbial cells, intriguing insights into organic matter transformation in the deep ocean emerged. On average, solute transporters accounted for 23{\%} of identified protein sequences in the lower euphotic and ∼39{\%} in the bathypelagic layer, indicating the central role of heterotrophy in the dark ocean. In the bathypelagic layer, substrate affinities of expressed transporters suggest that, in addition to amino acids, peptides and carbohydrates, carboxylic acids and compatible solutes may be essential substrates for the microbial community. Key players with highest expression of solute transporters were Alphaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria, accounting for 40{\%}, 11{\%}, and 10{\%}, respectively, of relative protein abundances. The in situ expression of solute transporters indicates that the heterotrophic prokaryotic community is geared toward the utilization of similar organic compounds throughout the water column, with yet higher abundances of transporters targeting aromatic compounds in the bathypelagic realm.",
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note = "Copyright {\circledC} 2018 the Author(s). Published by PNAS.",
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doi = "10.1073/pnas.1708779115",
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Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. / Bergauer, Kristin; Fernandez-Guerra, Antonio; Garcia, Juan A L; Sprenger, Richard R; Stepanauskas, Ramunas; Pachiadaki, Maria G; Jensen, Ole N; Herndl, Gerhard J.

I: Proceedings of the National Academy of Sciences of the United States of America, Bind 115, Nr. 3, 16.01.2018, s. E400-E408.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics

AU - Bergauer, Kristin

AU - Fernandez-Guerra, Antonio

AU - Garcia, Juan A L

AU - Sprenger, Richard R

AU - Stepanauskas, Ramunas

AU - Pachiadaki, Maria G

AU - Jensen, Ole N

AU - Herndl, Gerhard J

N1 - Copyright © 2018 the Author(s). Published by PNAS.

PY - 2018/1/16

Y1 - 2018/1/16

N2 - The phylogenetic composition of the heterotrophic microbial community is depth stratified in the oceanic water column down to abyssopelagic layers. In the layers below the euphotic zone, it has been suggested that heterotrophic microbes rely largely on solubilized particulate organic matter as a carbon and energy source rather than on dissolved organic matter. To decipher whether changes in the phylogenetic composition with depth are reflected in changes in the bacterial and archaeal transporter proteins, we generated an extensive metaproteomic and metagenomic dataset of microbial communities collected from 100- to 5,000-m depth in the Atlantic Ocean. By identifying which compounds of the organic matter pool are absorbed, transported, and incorporated into microbial cells, intriguing insights into organic matter transformation in the deep ocean emerged. On average, solute transporters accounted for 23% of identified protein sequences in the lower euphotic and ∼39% in the bathypelagic layer, indicating the central role of heterotrophy in the dark ocean. In the bathypelagic layer, substrate affinities of expressed transporters suggest that, in addition to amino acids, peptides and carbohydrates, carboxylic acids and compatible solutes may be essential substrates for the microbial community. Key players with highest expression of solute transporters were Alphaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria, accounting for 40%, 11%, and 10%, respectively, of relative protein abundances. The in situ expression of solute transporters indicates that the heterotrophic prokaryotic community is geared toward the utilization of similar organic compounds throughout the water column, with yet higher abundances of transporters targeting aromatic compounds in the bathypelagic realm.

AB - The phylogenetic composition of the heterotrophic microbial community is depth stratified in the oceanic water column down to abyssopelagic layers. In the layers below the euphotic zone, it has been suggested that heterotrophic microbes rely largely on solubilized particulate organic matter as a carbon and energy source rather than on dissolved organic matter. To decipher whether changes in the phylogenetic composition with depth are reflected in changes in the bacterial and archaeal transporter proteins, we generated an extensive metaproteomic and metagenomic dataset of microbial communities collected from 100- to 5,000-m depth in the Atlantic Ocean. By identifying which compounds of the organic matter pool are absorbed, transported, and incorporated into microbial cells, intriguing insights into organic matter transformation in the deep ocean emerged. On average, solute transporters accounted for 23% of identified protein sequences in the lower euphotic and ∼39% in the bathypelagic layer, indicating the central role of heterotrophy in the dark ocean. In the bathypelagic layer, substrate affinities of expressed transporters suggest that, in addition to amino acids, peptides and carbohydrates, carboxylic acids and compatible solutes may be essential substrates for the microbial community. Key players with highest expression of solute transporters were Alphaproteobacteria, Gammaproteobacteria, and Deltaproteobacteria, accounting for 40%, 11%, and 10%, respectively, of relative protein abundances. The in situ expression of solute transporters indicates that the heterotrophic prokaryotic community is geared toward the utilization of similar organic compounds throughout the water column, with yet higher abundances of transporters targeting aromatic compounds in the bathypelagic realm.

KW - Atlantic Ocean

KW - Deep sea

KW - Metaproteomics

KW - Organic matter

KW - Transporter proteins

U2 - 10.1073/pnas.1708779115

DO - 10.1073/pnas.1708779115

M3 - Journal article

VL - 115

SP - E400-E408

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 3

ER -