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Diazotroph Genomes and Their Seasonal Dynamics in a Stratified fmicb-11-01500 July 1, 2020 Time: 12:25 # 1 ORIGINAL RESEARCH published: 01 July 2020 doi: 10.3389/fmicb.2020.01500 Diazotroph Genomes and Their Seasonal Dynamics in a Stratified Humic Bog Lake Leyden Fernandez1, Sari Peura2, Alexander Eiler1,3, Alexandra M. Linz4, Katherine D. McMahon5,6 and Stefan Bertilsson1,7* 1 Department of Ecology and Genetics, Limnology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden, 2 Department of Forest Mycology and Plant Pathology, Science for Life Laboratory, Swedish University of Agricultural Sciences, Uppsala, Sweden, 3 Centre for Biogeochemistry in the Anthropocene, Department of Biosciences, Section for Aquatic Biology and Toxicology, University of Oslo, Oslo, Norway, 4 Great Lakes Bioenergy Research Center, Wisconsin Edited by: Energy Institute, University of Wisconsin–Madison, Madison, WI, United States, 5 Department of Bacteriology, University Sophie Rabouille, of Wisconsin–Madison, Madison, WI, United States, 6 Department of Civil and Environmental Engineering, University UMR7621 Laboratoire of Wisconsin–Madison, Madison, WI, United States, 7 Department of Aquatic Sciences and Assessment, Swedish University d’Océanographie Microbienne of Agricultural Sciences, Uppsala, Sweden (LOMIC), France Reviewed by: Aquatic N-fixation is generally associated with the growth and mass development Trinity L. Hamilton, University of Minnesota Twin Cities, of Cyanobacteria in nitrogen-deprived photic zones. However, sequenced genomes United States and environmental surveys suggest active aquatic N-fixation also by many non- Teresa Thiel, University of Missouri–St. Louis, cyanobacterial groups. Here, we revealed the seasonal variation and genomic diversity United States of potential N-fixers in a humic bog lake using metagenomic data and nif gene clusters Mary R. Gradoville, analysis. Groups with diazotrophic operons were functionally divergent and included University of California, Santa Cruz, United States Cholorobi, Geobacter, Desulfobacterales, Methylococcales, and Acidobacteria. In *Correspondence: addition to nifH (a gene that encodes the dinitrogenase reductase component of the Stefan Bertilsson molybdenum nitrogenase), we also identified sequences corresponding to vanadium [email protected] and iron-only nitrogenase genes. Within the Chlorobi population, the nitrogenase (nifH) Specialty section: cluster was included in a well-structured retrotransposon. Furthermore, the presence This article was submitted to of light-harvesting photosynthesis genes implies that anoxygenic photosynthesis may Aquatic Microbiology, a section of the journal fuel nitrogen fixation under the prevailing low-irradiance conditions. The presence Frontiers in Microbiology of rnf genes (related to the expression of HC/NaC-translocating ferredoxin: NADC Received: 16 October 2019 oxidoreductase) in Methylococcales and Desulfobacterales suggests that other energy- Accepted: 09 June 2020 generating processes may drive the costly N-fixation in the absence of photosynthesis. Published: 01 July 2020 The highly reducing environment of the anoxic bottom layer of Trout Bog Lake may Citation: Fernandez L, Peura S, Eiler A, thus also provide a suitable niche for active N-fixers and primary producers. While Linz AM, McMahon KD and future studies on the activity of these potential N-fixers are needed to clarify their role Bertilsson S (2020) Diazotroph Genomes and Their Seasonal in freshwater nitrogen cycling, the metagenomic data presented here enabled an initial Dynamics in a Stratified Humic Bog characterization of previously overlooked diazotrophs in freshwater biomes. Lake. Front. Microbiol. 11:1500. doi: 10.3389/fmicb.2020.01500 Keywords: diazotrophs, N-fixation, lake, hypolimnion, nifH gene Frontiers in Microbiology| www.frontiersin.org 1 July 2020| Volume 11| Article 1500 fmicb-11-01500 July 1, 2020 Time: 12:25 # 2 Fernandez et al. Non-cyanobacteria Freshwater Diazotrophs INTRODUCTION (Bombar et al., 2016). This contradicts observations in earlier studies, in which Cyanobacteria appeared responsible for Recent studies in deep marine waters have revealed active most planktonic N-fixation (Howarth et al., 1988) and may N-fixation and a wide diversity of non-cyanobacterial N-fixers point to less constrained regulation of diazotrophy among the (Farnelid et al., 2013; Bombar et al., 2016; Gradoville et al., heterotrophic N-fixers. 2017). The metabolic process by which atmospheric dinitrogen Many questions remain regarding the broader role of N-fixers gas (N2) is transformed to biologically more reactive forms in freshwater ecosystems, the identity of important diazotrophs, is known as diazotrophy (Howarth et al., 1988). Despite the and the metabolic traits enabling them to carry out the energy- ecological and biogeochemical significance of this process, there demanding N-fixation. A pioneering study in Lake George, is limited knowledge about the distribution of this trait in New York (Zani et al., 2000) attributed the active freshwater nifH different freshwater microorganisms. In particular, very little phylotypes mainly to unicellular and filamentous Cyanobacteria, is known about non-cyanobacterial diazotrophs in freshwater Alphaproteobacteria, and Gammaproteobacteria. A study carried systems, while at the same time, many of these ecosystems feature out by Halm et al.(2009) in the Lake Cadagno (Switzerland), steep redox gradients and anoxic zones that might provide unique reported for the first time that green sulfur bacteria (GSB), habitats for previously unrecognized N-fixers. namely, Chlorobi, could be involved in freshwater N-fixation. In Only select Archaea and Bacteria have the ability to this study, they also targeted nifH genes expressed as mRNA, transform and assimilate N2 gas, and the key enzyme to showing that N-fixers were more active at the chemocline. By mediate this process is the nitrogenase (Canfield et al., in situ hybridization-secondary ion mass spectroscopy, they 2010). Three nitrogenases co-exist in nature: molybdenum- further verified active diazotrophy in Chlorobi. Focusing on iron (Mo-nitrogenase), vanadium-iron, and iron-only (Fe-only deep lake sediments rather than the overlying waters, Parro nitrogenase). The corresponding gene clusters involved are et al.(2017) also recorded the presence of nitrogen fixation nifHDK (molybdenum-iron), vnfHGDK (vanadium-iron), and gene products using immunodetection and hypothesized that anfHGDK (Fe-only). Mo-nitrogenase is found in all diazotrophs, these were associated with non-cyanobacterial diazotrophs such and its expression is regulated by Mo concentration. Vanadium- as Azospira and Arcobacter seen in 16S rRNA inventories. iron nitrogenase is present in some microorganisms and may be Further, a phylogenetically diverse group of non-cyanobacterial expressed when Mo is scarce. The other alternative nitrogenase, diazotrophs was recently suggested to dominate N-fixation in Fe-only, has dual enzymatic functions and may simultaneously permafrost thaw ponds, and were possibly engaged in syntrophic reduce N2 and CO2 to CH4 and H2 in a single enzymatic step relationship with methanogenic Archaea residing in these ponds (Zheng et al., 2018). (Fernandez et al., 2019). However, many freshwater diazotrophs, As a result of metatranscriptomic oceanic surveys, significant particularly those inhabiting the darker waters of lakes, have expression of genes associated with N-fixation has been remained unexplored. found in water below the photic zone. This implies a hitherto Here, we studied the temporal dynamics of potential unrecognized non-cyanobacterial contribution to global marine diazotrophs by analyzing metagenomic sequence data and N-fixation. The N-fixation activity of these non-cyanobacterial environmental parameters from epilimnetic and hypolimnetic diazotrophs is typically associated with energy sources other waters of Trout Bog Lake (Wisconsin, United States), than oxygenic photosynthesis (Farnelid et al., 2013). With the representing a lake type typical for boreal regions. This introduction of new high-throughput sequencing technologies direct sequencing approach avoids the pitfalls and limitations and well-described marker genes such as nifH and nifD, introduced by primer coverage and other inevitable biases related the list of identified marine microorganisms potentially to PCR-based assays. The samples were collected from early capable of N-fixation has grown in recent years. For instance, spring to autumn across three consecutive years, providing the many proteobacterial diazotrophs (typically described as first broader account of the temporal dynamics of diazotrophs “heterotrophic N-fixers”) have been found to be abundant, in humic lakes. We also describe the main genomic features of widespread, and sometimes numerically dominant diazotrophs the most abundant diazotrophs in the anoxic bottom waters in the ocean (Bombar et al., 2016; Gradoville et al., 2017). In a (hypolimnion) of Trout Bog Lake by analyzing metagenome N-fixation study carried out across the chemocline of the central assembled genomes (MAGs). The thermal stratification in the Baltic Sea, two gammaproteobacterial-like nifH containing gene small and sheltered Trout Bog Lake is very stable during the clusters, EQF91 and ALHOU, were targeted by quantitative PCR warm period of the year. Furthermore, the water has high (qPCR) and could be associated to active N-fixation despite allochthonous dissolved organic carbon concentration, and thus, ample availability of bio-assimilable N compounds (Farnelid light penetration
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