Abstract
Diverse planktonic microorganisms play a crucial role in mediating methane flux from the ocean to the atmosphere. The distribution and composition of the marine methanotroph community is determined partly by oxygen availability. The low oxygen conditions of oxygen minimum zones (OMZs) may select for methanotrophs that oxidize methane using inorganic nitrogen compounds (e.g., nitrate, nitrite) in place of oxygen. However, environmental evidence for methane-nitrogen linkages in OMZs remains sparse, as does our knowledge of the genomic content and metabolic capacity of organisms catalyzing OMZ methane oxidation. Here, binning of metagenome sequences from a coastal anoxic OMZ recovered the first near complete (95%) draft genome representing the methanotroph clade OPU3. Phylogenetic reconstruction of concatenated single copy marker genes confirmed the OPU3-like bacterium as a divergent member of the type Ia methanotrophs, with an estimated genome size half that of other sequenced taxa in this group. The proportional abundance of this bacterium peaked at 4% of the total microbial community at the top of the anoxic zone in areas of nitrite and nitrate availability but declining methane concentrations. Genes mediating dissimilatory nitrate and nitrite reduction were identified in the OPU3 genome, and transcribed in conjunction with key enzymes catalyzing methane oxidation to formaldehyde and the ribulose monophosphate (RuMP) pathway for formaldehyde assimilation, suggesting partial denitrification linked to methane oxidation. Together, these data provide the first field-based evidence for methanotrophic partial denitrification by the OPU3 cluster under anoxic conditions, supporting a role for OMZs as key sites in pelagic methane turnover.
Highlights
Methane (CH4) is a potent greenhouse gas with 25 times the warming potential per-mol compared to CO2 (IPCC, 2013)
Eight of these operational taxonomic units (OTUs) remained after rarefaction (3844 reads) of the total gDNA and community DNA (gDNA) and RNA (cDNA) amplicon pools
One OTU from the OPU1 clade (GD_791) was detected and was confined primarily to the 60 m sample where O2 concentration was ∼25 μM. These eight OTUs, which collectively represented 1.8% of the total gDNA combined over all depths, were undetected or at low abundance (0.4%) above or within the oxycline (30 and 60 m, respectively) but increased to 4–5% of the gDNA pool in the upper anoxic zone (90 and 100 m) where O2 concentrations fell below detection,
Summary
Methane (CH4) is a potent greenhouse gas with 25 times the warming potential per-mol compared to CO2 (IPCC, 2013). Methane production has been observed under both oxic and anoxic conditions, the mechanisms of production differ, via either archaeal methanogenesis in sediments (Reeburgh, 2007; Valentine, 2011) or aerobic catabolism of methylated phosphorous-containing compounds (Karl et al, 2008; Damm et al, 2010; Carini et al, 2014). The metabolic pathways used to consume methane include both aerobic methanotrophy and anaerobic oxidation of methane (AOM). The latter process is mediated by prokaryotes using alternative oxidants such aapsnudtsautnilvfiaetrteigtee(nSe(ONra24Ot−io−2; n;KoRnfaitgitnehtloraeacbneadlrlsuiBlnaogretoeixutysg,ael.2n,002fr90o)0m6o; rnEittthrtwartoiegu(gNehtOta−3hl.e), 2010). While marine methanotrophy has been studied extensively over the past decades (Reeburgh, 2007; Valentine, 2011), the variables controlling the diversity, distribution, and activity of the dominant pelagic methanotrophs are still not well-understood, and genomic data for the diverse members of the marine methanotroph community remain sparse
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