Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake

Aquatic N-fixation is generally associated with the growth and mass development of Cyanobacteria in nitrogen-deprived photic zones. However, sequenced genomes and environmental surveys suggest active aquatic N-fixation also by many non-cyanobacterial groups. Here, we revealed the seasonal variation...

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Main Authors: Leyden Fernandez, Sari Peura, Alexander Eiler, Alexandra M. Linz, Katherine D. McMahon, Stefan Bertilsson
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.01500/full
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spelling doaj-acc3950b65644b2cb513cccf2fa2576c2020-11-25T03:43:38ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01500505352Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog LakeLeyden Fernandez0Sari Peura1Alexander Eiler2Alexander Eiler3Alexandra M. Linz4Katherine D. McMahon5Katherine D. McMahon6Stefan Bertilsson7Stefan Bertilsson8Department of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, SwedenDepartment of Forest Mycology and Plant Pathology, Science for Life Laboratory, Swedish University of Agricultural Sciences, Uppsala, SwedenDepartment of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, SwedenCentre for Biogeochemistry in the Anthropocene, Department of Biosciences, Section for Aquatic Biology and Toxicology, University of Oslo, Oslo, NorwayGreat Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin–Madison, Madison, WI, United StatesDepartment of Bacteriology, University of Wisconsin–Madison, Madison, WI, United StatesDepartment of Civil and Environmental Engineering, University of Wisconsin–Madison, Madison, WI, United StatesDepartment of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, SwedenDepartment of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences, Uppsala, SwedenAquatic N-fixation is generally associated with the growth and mass development of Cyanobacteria in nitrogen-deprived photic zones. However, sequenced genomes and environmental surveys suggest active aquatic N-fixation also by many non-cyanobacterial groups. Here, we revealed the seasonal variation and genomic diversity of potential N-fixers in a humic bog lake using metagenomic data and nif gene clusters analysis. Groups with diazotrophic operons were functionally divergent and included Cholorobi, Geobacter, Desulfobacterales, Methylococcales, and Acidobacteria. In addition to nifH (a gene that encodes the dinitrogenase reductase component of the molybdenum nitrogenase), we also identified sequences corresponding to vanadium and iron-only nitrogenase genes. Within the Chlorobi population, the nitrogenase (nifH) cluster was included in a well-structured retrotransposon. Furthermore, the presence of light-harvesting photosynthesis genes implies that anoxygenic photosynthesis may fuel nitrogen fixation under the prevailing low-irradiance conditions. The presence of rnf genes (related to the expression of H+/Na+-translocating ferredoxin: NAD+ oxidoreductase) in Methylococcales and Desulfobacterales suggests that other energy-generating processes may drive the costly N-fixation in the absence of photosynthesis. The highly reducing environment of the anoxic bottom layer of Trout Bog Lake may thus also provide a suitable niche for active N-fixers and primary producers. While future studies on the activity of these potential N-fixers are needed to clarify their role in freshwater nitrogen cycling, the metagenomic data presented here enabled an initial characterization of previously overlooked diazotrophs in freshwater biomes.https://www.frontiersin.org/article/10.3389/fmicb.2020.01500/fulldiazotrophsN-fixationlakehypolimnionnifH gene
collection DOAJ
language English
format Article
sources DOAJ
author Leyden Fernandez
Sari Peura
Alexander Eiler
Alexander Eiler
Alexandra M. Linz
Katherine D. McMahon
Katherine D. McMahon
Stefan Bertilsson
Stefan Bertilsson
spellingShingle Leyden Fernandez
Sari Peura
Alexander Eiler
Alexander Eiler
Alexandra M. Linz
Katherine D. McMahon
Katherine D. McMahon
Stefan Bertilsson
Stefan Bertilsson
Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake
Frontiers in Microbiology
diazotrophs
N-fixation
lake
hypolimnion
nifH gene
author_facet Leyden Fernandez
Sari Peura
Alexander Eiler
Alexander Eiler
Alexandra M. Linz
Katherine D. McMahon
Katherine D. McMahon
Stefan Bertilsson
Stefan Bertilsson
author_sort Leyden Fernandez
title Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake
title_short Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake
title_full Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake
title_fullStr Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake
title_full_unstemmed Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake
title_sort diazotroph genomes and their seasonal dynamics in a stratified humic bog lake
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-07-01
description Aquatic N-fixation is generally associated with the growth and mass development of Cyanobacteria in nitrogen-deprived photic zones. However, sequenced genomes and environmental surveys suggest active aquatic N-fixation also by many non-cyanobacterial groups. Here, we revealed the seasonal variation and genomic diversity of potential N-fixers in a humic bog lake using metagenomic data and nif gene clusters analysis. Groups with diazotrophic operons were functionally divergent and included Cholorobi, Geobacter, Desulfobacterales, Methylococcales, and Acidobacteria. In addition to nifH (a gene that encodes the dinitrogenase reductase component of the molybdenum nitrogenase), we also identified sequences corresponding to vanadium and iron-only nitrogenase genes. Within the Chlorobi population, the nitrogenase (nifH) cluster was included in a well-structured retrotransposon. Furthermore, the presence of light-harvesting photosynthesis genes implies that anoxygenic photosynthesis may fuel nitrogen fixation under the prevailing low-irradiance conditions. The presence of rnf genes (related to the expression of H+/Na+-translocating ferredoxin: NAD+ oxidoreductase) in Methylococcales and Desulfobacterales suggests that other energy-generating processes may drive the costly N-fixation in the absence of photosynthesis. The highly reducing environment of the anoxic bottom layer of Trout Bog Lake may thus also provide a suitable niche for active N-fixers and primary producers. While future studies on the activity of these potential N-fixers are needed to clarify their role in freshwater nitrogen cycling, the metagenomic data presented here enabled an initial characterization of previously overlooked diazotrophs in freshwater biomes.
topic diazotrophs
N-fixation
lake
hypolimnion
nifH gene
url https://www.frontiersin.org/article/10.3389/fmicb.2020.01500/full
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