Dissolved oxygen concentrations influence microbial community structure and key players in an oxygen minimum zone.

Abstract

Oxygen minimum zones (OMZs) are expanding in the global ocean. Declining oxygen can alter microbial processes that regulate carbon, nitrogen, and sulfur cycling, including pathways with the potential to produce nitrous oxide (N₂O), a potent greenhouse gas. Yet, we lack a full understanding of how microbial communities respond to declining oxygen in some globally important OMZs. This is particularly true for the understudied northern Benguela Upwelling System (nBUS), an important source of marine N₂O. Here, we analyzed the influence of oxygen concentrations on microbial communities in the nBUS OMZ using 16S rRNA gene sequence data. Microbial diversity did not decline linearly with oxygen and was highest under dysoxic (0.2-2.0 mL/L) conditions and lowest under suboxic (0.0-0.2 mL/L) conditions. This pattern was primarily due to changes in community evenness, which decreased in suboxic samples as the relative abundance of Thioglobaceae (SUP05) increased. Thioglobaceae relative abundance was significantly inversely correlated with oxygen, and Thioglobaceae were abundant in the nBUS OMZ. Analysis of 216 publicly available medium- to high-quality Thioglobaceae genomes from cultured and uncultured microbes sampled in the nBUS and other OMZs revealed the metabolic potential of this clade for carbon fixation and consumption, sulfur oxidation, and denitrification. Importantly, few Thioglobaceae possess the genetic potential to carry out complete denitrification as most lack the gene that converts N₂O to dinitrogen gas. As OMZs expand in size and severity, decreasing microbial diversity and a concomitant increase in the relative abundance of Thioglobaceae could contribute to enhanced N₂O production through incomplete denitrification.IMPORTANCEMarine microbes mediate biogeochemical cycles, which are influenced by oxygen concentrations, including microbial pathways that can lead to nitrous oxide (N₂O) production. The oxygen minimum zone (OMZ) in the northern Benguela Upwelling System (nBUS) is a biogeochemical hotspot and an important source of nitrous oxide. Yet, microbial community responses remain poorly characterized in this understudied OMZ. Analysis of microbial communities in this OMZ, combined with comparative genomic analysis of Thioglobaceae from the global ocean, revealed that members of this group have the capacity to fix carbon, potentially supporting growth through sulfur oxidation coupled to denitrification. However, few Thioglobaceae have the genetic potential to carry out complete denitrification, with the final nitrous oxide reduction step often missing. Incomplete denitrification is an important source of N₂O in OMZs. Collectively, this study linked oxygen-associated community shifts in this OMZ to incomplete denitrification in a microbial group that increased in relative abundance as oxygen declined.