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Title: Genome Streamlining, Proteorhodopsin, and Organic Nitrogen Metabolism in Freshwater Nitrifiers

Abstract

Microbial nitrification is a critical process governing nitrogen availability in aquatic systems. Freshwater nitrifiers have received little attention, leaving many unanswered questions about their taxonomic distribution, functional potential, and ecological interactions. Here, we reconstructed genomes to infer the metabolism and ecology of free-living picoplanktonic nitrifiers across the Laurentian Great Lakes, a connected series of five of Earth’s largest lakes. Surprisingly, ammonia-oxidizing bacteria (AOB) related to Nitrosospira dominated over ammonia-oxidizing archaea (AOA) at nearly all stations, with distinct ecotypes prevailing in the transparent, oligotrophic upper lakes compared to Lakes Erie and Ontario. Unexpectedly, one ecotype of Nitrosospira encodes proteorhodopsin, which could enhance survival under conditions where ammonia oxidation is inhibited or substrate limited. Nitrite-oxidizing bacteria (NOB) “Candidatus Nitrotoga” and Nitrospira fluctuated in dominance, with the latter prevailing in deeper, less-productive basins. Genome reconstructions reveal highly reduced genomes and features consistent with genome streamlining, along with diverse adaptations to sunlight and oxidative stress and widespread capacity for organic nitrogen use. Our findings expand the known functional diversity of nitrifiers and establish their ecological genomics in large lake ecosystems. By elucidating links between microbial biodiversity and biogeochemical cycling, our work also informs ecosystem models of the Laurentian Great Lakes, a critical freshwater resourcemore » experiencing rapid environmental change.« less

Authors:
 [1];  [1];  [2]; ORCiD logo [1]
  1. University of Chicago, IL (United States)
  2. University of Wisconsin, Madison, WI (United States)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Illinois-Indiana Sea Grant; UChicago Women’s Board; National Science Foundation (NSF)
OSTI Identifier:
1904118
Grant/Contract Number:  
AC02-05CH11231; NA14OAR170095; OCE-1830011
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 13; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biogeochemistry; ecological genomics; freshwater; metagenomics; nitrification

Citation Formats

Podowski, Justin C., Paver, Sara F., Newton, Ryan J., and Coleman, Maureen L. Genome Streamlining, Proteorhodopsin, and Organic Nitrogen Metabolism in Freshwater Nitrifiers. United States: N. p., 2022. Web. doi:10.1128/mbio.02379-21.
Podowski, Justin C., Paver, Sara F., Newton, Ryan J., & Coleman, Maureen L. Genome Streamlining, Proteorhodopsin, and Organic Nitrogen Metabolism in Freshwater Nitrifiers. United States. https://doi.org/10.1128/mbio.02379-21
Podowski, Justin C., Paver, Sara F., Newton, Ryan J., and Coleman, Maureen L. Mon . "Genome Streamlining, Proteorhodopsin, and Organic Nitrogen Metabolism in Freshwater Nitrifiers". United States. https://doi.org/10.1128/mbio.02379-21. https://www.osti.gov/servlets/purl/1904118.
@article{osti_1904118,
title = {Genome Streamlining, Proteorhodopsin, and Organic Nitrogen Metabolism in Freshwater Nitrifiers},
author = {Podowski, Justin C. and Paver, Sara F. and Newton, Ryan J. and Coleman, Maureen L.},
abstractNote = {Microbial nitrification is a critical process governing nitrogen availability in aquatic systems. Freshwater nitrifiers have received little attention, leaving many unanswered questions about their taxonomic distribution, functional potential, and ecological interactions. Here, we reconstructed genomes to infer the metabolism and ecology of free-living picoplanktonic nitrifiers across the Laurentian Great Lakes, a connected series of five of Earth’s largest lakes. Surprisingly, ammonia-oxidizing bacteria (AOB) related to Nitrosospira dominated over ammonia-oxidizing archaea (AOA) at nearly all stations, with distinct ecotypes prevailing in the transparent, oligotrophic upper lakes compared to Lakes Erie and Ontario. Unexpectedly, one ecotype of Nitrosospira encodes proteorhodopsin, which could enhance survival under conditions where ammonia oxidation is inhibited or substrate limited. Nitrite-oxidizing bacteria (NOB) “Candidatus Nitrotoga” and Nitrospira fluctuated in dominance, with the latter prevailing in deeper, less-productive basins. Genome reconstructions reveal highly reduced genomes and features consistent with genome streamlining, along with diverse adaptations to sunlight and oxidative stress and widespread capacity for organic nitrogen use. Our findings expand the known functional diversity of nitrifiers and establish their ecological genomics in large lake ecosystems. By elucidating links between microbial biodiversity and biogeochemical cycling, our work also informs ecosystem models of the Laurentian Great Lakes, a critical freshwater resource experiencing rapid environmental change.},
doi = {10.1128/mbio.02379-21},
journal = {mBio (Online)},
number = 3,
volume = 13,
place = {United States},
year = {Mon Apr 18 00:00:00 EDT 2022},
month = {Mon Apr 18 00:00:00 EDT 2022}
}

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Fast gapped-read alignment with Bowtie 2
journal, March 2012

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Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper
journal, April 2017

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BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era
journal, February 2020

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BLAST+: architecture and applications
journal, January 2009

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Comparison of Oxidation Kinetics of Nitrite-Oxidizing Bacteria: Nitrite Availability as a Key Factor in Niche Differentiation
journal, November 2014

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Cultivation and Transcriptional Analysis of a Canonical Nitrospira Under Stable Growth Conditions
journal, June 2019

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High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries
journal, November 2018


Proteorhodopsin phototrophy in the ocean
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Low Temperature and Neutral pH Define “ Candidatus Nitrotoga sp.” as a Competitive Nitrite Oxidizer in Coculture with Nitrospira defluvii
journal, May 2019

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Photoinactivation of Ammonia Oxidation in Nitrosomonas
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DNA deaminating ability and genotoxicity of nitric oxide and its progenitors
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Ammonia and Nitrate Uptake in the Lower Great Lakes
journal, September 1980

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Rates and controls of nitrification in a large oligotrophic lake
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Isolation of single-site Escherichia coli mutants deficient in thiamine and 4-thiouridine syntheses: identification of a nuvC mutant
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Spatiotemporal distribution of bacterioplankton functional groups along a freshwater estuary to pelagic gradient in Lake Michigan
journal, October 2016

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The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium
journal, May 2013


NCBI prokaryotic genome annotation pipeline
journal, June 2016

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Phosphorus and trace metal limitation of algae and bacteria in Lake Superior
journal, March 2004

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Ecosystem services of Earth’s largest freshwater lakes
journal, February 2020


Growth at Low Ammonium Concentrations and Starvation Response as Potential Factors Involved in Niche Differentiation among Ammonia-Oxidizing Bacteria
journal, October 2002

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Long-term trends of nutrients and trophic response variables for the Great Lakes
journal, February 2015

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Protonation State of Glu142 Differs in the Green- and Blue-Absorbing Variants of Proteorhodopsin
journal, February 2008

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