Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”

ABSTRACT Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called “dead zones,” are increasing in number and severity around the globe with deleterious effects on ecology and economics. One of the largest of these coastal dead zones occurs on the cont...

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Autores principales:	J. Cameron Thrash, Kiley W. Seitz, Brett J. Baker, Ben Temperton, Lauren E. Gillies, Nancy N. Rabalais, Bernard Henrissat, Olivia U. Mason
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	candidate phyla hypoxia metagenomics microbial ecology microbial metabolism Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/274951523a3544a0bc94fd00bacb31ca
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spelling	oai:doaj.org-article:274951523a3544a0bc94fd00bacb31ca2021-11-15T15:51:51ZMetabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”10.1128/mBio.01017-172150-7511https://doaj.org/article/274951523a3544a0bc94fd00bacb31ca2017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01017-17https://doaj.org/toc/2150-7511ABSTRACT Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called “dead zones,” are increasing in number and severity around the globe with deleterious effects on ecology and economics. One of the largest of these coastal dead zones occurs on the continental shelf of the northern Gulf of Mexico (nGOM), which results from eutrophication-enhanced bacterioplankton respiration and strong seasonal stratification. Previous research in this dead zone revealed the presence of multiple cosmopolitan bacterioplankton lineages that have eluded cultivation, and thus their metabolic roles in this ecosystem remain unknown. We used a coupled shotgun metagenomic and metatranscriptomic approach to determine the metabolic potential of Marine Group II Euryarchaeota, SAR406, and SAR202. We recovered multiple high-quality, nearly complete genomes from all three groups as well as candidate phyla usually associated with anoxic environments—Parcubacteria (OD1) and Peregrinibacteria. Two additional groups with putative assignments to ACD39 and PAUC34f supplement the metabolic contributions by uncultivated taxa. Our results indicate active metabolism in all groups, including prevalent aerobic respiration, with concurrent expression of genes for nitrate reduction in SAR406 and SAR202, and dissimilatory nitrite reduction to ammonia and sulfur reduction by SAR406. We also report a variety of active heterotrophic carbon processing mechanisms, including degradation of complex carbohydrate compounds by SAR406, SAR202, ACD39, and PAUC34f. Together, these data help constrain the metabolic contributions from uncultivated groups in the nGOM during periods of low DO and suggest roles for these organisms in the breakdown of complex organic matter. IMPORTANCE Dead zones receive their name primarily from the reduction of eukaryotic macrobiota (demersal fish, shrimp, etc.) that are also key coastal fisheries. Excess nutrients contributed from anthropogenic activity such as fertilizer runoff result in algal blooms and therefore ample new carbon for aerobic microbial metabolism. Combined with strong stratification, microbial respiration reduces oxygen in shelf bottom waters to levels unfit for many animals (termed hypoxia). The nGOM shelf remains one of the largest eutrophication-driven hypoxic zones in the world, yet despite its potential as a model study system, the microbial metabolisms underlying and resulting from this phenomenon—many of which occur in bacterioplankton from poorly understood lineages—have received only preliminary study. Our work details the metabolic potential and gene expression activity for uncultivated lineages across several low DO sites in the nGOM, improving our understanding of the active biogeochemical cycling mediated by these “microbial dark matter” taxa during hypoxia.J. Cameron ThrashKiley W. SeitzBrett J. BakerBen TempertonLauren E. GilliesNancy N. RabalaisBernard HenrissatOlivia U. MasonAmerican Society for Microbiologyarticlecandidate phylahypoxiametagenomicsmicrobial ecologymicrobial metabolismMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	candidate phyla hypoxia metagenomics microbial ecology microbial metabolism Microbiology QR1-502
spellingShingle	candidate phyla hypoxia metagenomics microbial ecology microbial metabolism Microbiology QR1-502 J. Cameron Thrash Kiley W. Seitz Brett J. Baker Ben Temperton Lauren E. Gillies Nancy N. Rabalais Bernard Henrissat Olivia U. Mason Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”
description	ABSTRACT Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called “dead zones,” are increasing in number and severity around the globe with deleterious effects on ecology and economics. One of the largest of these coastal dead zones occurs on the continental shelf of the northern Gulf of Mexico (nGOM), which results from eutrophication-enhanced bacterioplankton respiration and strong seasonal stratification. Previous research in this dead zone revealed the presence of multiple cosmopolitan bacterioplankton lineages that have eluded cultivation, and thus their metabolic roles in this ecosystem remain unknown. We used a coupled shotgun metagenomic and metatranscriptomic approach to determine the metabolic potential of Marine Group II Euryarchaeota, SAR406, and SAR202. We recovered multiple high-quality, nearly complete genomes from all three groups as well as candidate phyla usually associated with anoxic environments—Parcubacteria (OD1) and Peregrinibacteria. Two additional groups with putative assignments to ACD39 and PAUC34f supplement the metabolic contributions by uncultivated taxa. Our results indicate active metabolism in all groups, including prevalent aerobic respiration, with concurrent expression of genes for nitrate reduction in SAR406 and SAR202, and dissimilatory nitrite reduction to ammonia and sulfur reduction by SAR406. We also report a variety of active heterotrophic carbon processing mechanisms, including degradation of complex carbohydrate compounds by SAR406, SAR202, ACD39, and PAUC34f. Together, these data help constrain the metabolic contributions from uncultivated groups in the nGOM during periods of low DO and suggest roles for these organisms in the breakdown of complex organic matter. IMPORTANCE Dead zones receive their name primarily from the reduction of eukaryotic macrobiota (demersal fish, shrimp, etc.) that are also key coastal fisheries. Excess nutrients contributed from anthropogenic activity such as fertilizer runoff result in algal blooms and therefore ample new carbon for aerobic microbial metabolism. Combined with strong stratification, microbial respiration reduces oxygen in shelf bottom waters to levels unfit for many animals (termed hypoxia). The nGOM shelf remains one of the largest eutrophication-driven hypoxic zones in the world, yet despite its potential as a model study system, the microbial metabolisms underlying and resulting from this phenomenon—many of which occur in bacterioplankton from poorly understood lineages—have received only preliminary study. Our work details the metabolic potential and gene expression activity for uncultivated lineages across several low DO sites in the nGOM, improving our understanding of the active biogeochemical cycling mediated by these “microbial dark matter” taxa during hypoxia.
format	article
author	J. Cameron Thrash Kiley W. Seitz Brett J. Baker Ben Temperton Lauren E. Gillies Nancy N. Rabalais Bernard Henrissat Olivia U. Mason
author_facet	J. Cameron Thrash Kiley W. Seitz Brett J. Baker Ben Temperton Lauren E. Gillies Nancy N. Rabalais Bernard Henrissat Olivia U. Mason
author_sort	J. Cameron Thrash
title	Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”
title_short	Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”
title_full	Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”
title_fullStr	Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”
title_full_unstemmed	Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”
title_sort	metabolic roles of uncultivated bacterioplankton lineages in the northern gulf of mexico “dead zone”
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/274951523a3544a0bc94fd00bacb31ca
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Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone”

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