Dissolved oxygen concentrations influence microbial diversity, abundance and dominant players in an oxygen minimum zone

Abstract

Expansion of marine global oxygen minimum zones (OMZs) can have profound impacts on resident macrofauna. Less obvious is the influence OMZs will have on the diversity and abundance of planktonic microbes. This is particularly true in understudied OMZs such as the northern Benguela Upwelling System (nBUS). Here, we analyzed the influence of oxygen concentrations on the microbial community in the nBUS OMZ using 16S rRNA gene (iTag) sequence data. In the nBUS oxygen was a primary driver influencing microbial community structure and diversity. Diversity was highest in dysoxic samples and lowest in suboxic samples, which was primarily due to changes in community evenness in relationship to oxygen concentrations. For example, evenness decreased in suboxic samples due to oscillations in the abundance of microbial groups such as Thioglobaceae (SUP05), which was found to be the most abundant microbe in the nBUS OMZ and significantly increased in abundance as oxygen decreased. This finding prompted an analysis of 217 publicly available medium to high quality Thioglobaceae genomes, including cultured representatives, from the nBUS and other OMZs. Genome annotation of these Thioglobaceae indicated important roles in carbon cycling, sulfur oxidation and denitrification. Importantly, few Thioglobaceae possess the genetic potential to carry out complete denitrification, as most lack the gene that codes for nitrous oxide reductase (NosZ), which converts nitrous oxide (N2O), a potent greenhouse gas, to nitrogen gas. As OMZs expand in size and severity, decreasing microbial diversity and a concomitant increase in Thioglobaceae abundances, could lead to enhanced N2O production through incomplete denitrification. ImportanceHere, we found that microbial diversity decreased significantly with declining oxygen concentrations in the nBUS OMZ. However, one microbial group, the Thioglobaceae, was most abundant when oxygen was lowest. This group is able to support its growth through sulfur oxidation using either oxygen or nitrate (denitrification). A comprehensive genomic analysis of Thioglobaceae in the nBUS and in the global ocean revealed that few have the capacity to carry out complete denitrification, with the final step in this process often missing in these genomes. This incomplete pathway is consequential, as it can be an important source of nitrous oxide, particularly in marine OMZs such as the understudied nBUS. Collectively, this study provides new information on an OMZ, and definitively links an important microbial pathway, incomplete denitrification, to a particular and highly abundant group of microbes that appear to have a strong response to declining oxygen concentrations in the marine environment.