Environmental Microbiology
Research Article
6 March 2024

Novel Alphaproteobacteria transcribe genes for nitric oxide transformation at high levels in a marine oxygen-deficient zone

ABSTRACT

Marine oxygen-deficient zones (ODZs) are portions of the ocean where intense nitrogen loss occurs primarily via denitrification and anammox. Despite many decades of study, the identity of the microbes that catalyze nitrogen loss in ODZs is still being elucidated. Intriguingly, high transcription of genes in the same family as the nitric oxide dismutase (nod) gene from Methylomirabilota has been reported in the anoxic core of ODZs. Here, we show that the most abundantly transcribed nod genes in the Eastern Tropical North Pacific ODZ belong to a new order (UBA11136) of Alphaproteobacteria, rather than Methylomirabilota as previously assumed. Gammaproteobacteria and Planctomycetia also transcribe nod, but at lower relative abundance than UBA11136 in the upper ODZ. The nod-transcribing Alphaproteobacteria likely use formaldehyde and formate as a source of electrons for aerobic respiration, with additional electrons possibly from sulfide oxidation. They also transcribe multiheme cytochrome (here named ptd) genes for a putative porin-cytochrome protein complex of unknown function, potentially involved in extracellular electron transfer. Molecular oxygen for aerobic respiration may originate from nitric oxide dismutation via cryptic oxygen cycling. Our results implicate Alphaproteobacteria order UBA11136 as a significant player in marine nitrogen loss and highlight their potential in one-carbon, nitrogen, and sulfur metabolism in ODZs.

IMPORTANCE

In marine oxygen-deficient zones (ODZs), microbes transform bioavailable nitrogen to gaseous nitrogen, with nitric oxide as a key intermediate. The Eastern Tropical North Pacific contains the world’s largest ODZ, but the identity of the microbes transforming nitric oxide remains unknown. Here, we show that highly transcribed nitric oxide dismutase (nod) genes belong to Alphaproteobacteria of the novel order UBA11136, which lacks cultivated isolates. These Alphaproteobacteria show evidence for aerobic respiration, using oxygen potentially sourced from nitric oxide dismutase, and possess a novel porin-cytochrome protein complex with unknown function. Gammaproteobacteria and Planctomycetia transcribe nod at lower levels. Our results pinpoint the microbes mediating a key step in marine nitrogen loss and reveal an unexpected predicted metabolism for marine Alphaproteobacteria.

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Information & Contributors

Information

Published In

cover image Applied and Environmental Microbiology
Applied and Environmental Microbiology
Volume 90Number 417 April 2024
eLocator: e02099-23
Editor: Jennifer F. Biddle, University of Delaware, Newark, Delaware, USA
PubMed: 38445905

History

Received: 20 November 2023
Accepted: 9 February 2024
Published online: 6 March 2024

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Keywords

  1. nitric oxide
  2. Alphaproteobacteria
  3. marine
  4. oxygen-deficient zone
  5. nitrogen
  6. oxygen
  7. denitrification

Data Availability

The KBase bioinformatic pipeline and MAGs are at https://narrative.kbase.us/narrative/106999. Original metagenomic reads are available at BioProject PRJNA375524 (ETNP201306SV43, SAMN06344130) and BioProject PRJNA375542 (ETNP201310SV72, SAMN06344148). MAG Alphaproteobacteria bacterium ETNP2013_S06_300m_15 was deposited into BioProject PRJNA375524 (BioSample SAMN38229257, WGS Accession JAZDBU000000000) and Alphaproteobacteria bacterium ETNP2013_S10_300m_22 was deposited into BioProject PRJNA375542 (BioSample SAMN38228782, WGS Accession JAZDCE000000000). All ETNP ODZ data sets used in this manuscript are listed in Table S9.

Contributors

Authors

School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
Author Contributions: Formal analysis, Investigation, Methodology, and Visualization.
Department of Microbiology & Cell Biology, Montana State University, Bozeman, Montana, USA
Author Contributions: Funding acquisition and Writing – review and editing.
School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
Author Contributions: Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Visualization, Writing – original draft, and Writing – review and editing.

Editor

Jennifer F. Biddle
Editor
University of Delaware, Newark, Delaware, USA

Notes

The authors declare no conflict of interest.

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