Global Survey of Oxygen Minimum Zones Reveals Endemism and Functional Redundancy in Viral Communities

Abstract:

Marine oxygen minimum zones (OMZs) harbor distinct microbes that significantly affect global carbon, nitrogen, and sulfur cycles. It is thus imperative that we understand microbial community structure and function within these OMZs as they expand due to global climate change. Within the global oceans, it is evident that viruses alter the flow of carbon and nutrients both directly via host cell lysis and indirectly via the modulation of host cell physiology, which includes encoding for biogeochemically relevant genes (AMGs; Auxiliary Metabolic Genes) such as photosynthetic photosystem genes and nitrification genes. Despite this clear importance of both OMZs and viruses to global cycles, relatively few studies have been conducted regarding the diversity and genetic potential of viruses in OMZs and none have compared viruses between different OMZs. To address this, we used 56 viromes from samples collected across 5 OMZs spanning the global oceans to survey the diversity of viruses and their AMGs. Our results show high endemism within these OMZs, in which only 6 virus populations were present at every OMZ and ~67 % of the virus populations occurred within only a single OMZ. Further, our analyses did show that the 3 anoxic marine zones (AMZs; Eastern North and South Subtropical Pacific and Arabian Sea) were more similar to each other than they were to the other OMZs, but these AMZs shared only ~6 % of their viral populations. Even with the clear population endemism, the functional genetic potentials of the viral communities were, in general, highly similar between regions, including AMGs that encode for carbohydrate metabolism, respiration, and amino acid metabolism. However, other AMGs, including some AMGs related to nitrogen and sulfur cycling, were present within only one or two OMZs. Likewise, NMDS analyses of protein families and AMGs showed significant differences between regions. Altogether, these results indicate that there is little overlap between viral communities in separate marine OMZs, that there is some degree of functional redundancy for viral-encoded AMGs related to basal host metabolism, and that the viruses in each OMZ region have different AMG-related influences on global biogeochemical cycles.