Microbial Ecology under Ocean Deoxygenation: Diversity, Metabolisms, Environmental Controls

Oxygen minimum zones (OMZs) in the global oceans are formed and sustained by the complex interaction between biological processes of consumption and production, as well as physical supply mechanisms. Deoxygenation and continuous OMZ expansion point to a growing significant role of OMZ microbes in global biogeochemical cycles. However, comprehensive analysis and comparison of key cycles performed by microbial communities within marine OMZs and non-OMZ environments over large timescales or broad regional scales are currently lacking.

This thesis studied the microbial diversity, distribution, and their key metabolisms under ocean deoxygenation with different focuses in three large oceanic OMZs: the Tropical South Atlantic (TSA, Manuscript Ⅰ), the Eastern Tropical Pacific (ETP, Manuscript Ⅱ), and the Baltic Sea (Manuscript Ⅲ). Manuscript Ⅰ revealed a negative correlation between oxygen/nitrite levels and the prevalence of most nitrogen pathways (e.g., nitrate reduction and nitrite oxidation, nitrification, and denitrification (N2O production)), carbon pathways (e.g., CO oxidation and methanogenesis), phosphorus pathways (e.g., alkaline phosphatase), and sulfur pathways (e.g., sulfide oxidation). These pathways tended to exhibit higher abundances when the OMZs expand and upwelling turns more frequent or stronger in the TSA. Certain predominant drivers (e.g., SAR11, Nitrospina, Thermoproteota) and their genetic potentials were emphasized. Both the relative abundance of pathways of N2O consumption and production showed positive correlations with N2O content. Manuscript Ⅱ involved the temporal scale for studying the OMZ expansion and ENSO events on microbial diversity and metabolisms in the ETP. Despite the occurrence of multiple ENSO events from 2011-2022, including a strong El Niño in 2015- 2016, there appeared to be minimal variations in microbial diversity or taxonomy in the ETP. However, we did observe a significant decrease in the relative abundance of SAR11, accompanied by an increase in the potential for nitrogen metabolisms, such as denitrification (N2O production) and nitrogen fixation, both in the euphotic layer and the core of the OMZ. Moreover, the microbial abundance and some metabolisms (e.g., phosphate transport and regulation, nitrogen fixation) decreases but majority of nitrogen metabolisms increase along the oxygen gradient from oxic to suboxic. Distinct microbial dominant groups participating in essential biogeochemical cycles exhibited varying sensitivities to oxygen levels, and noticeable shifts in numerous functional groups were observed at oxygen thresholds of 120, 90, 80, 60, and 12 µmol/kg. Furthermore, the relative abundance of Thermoproteota encoding nitrite reductase (nirK) was positively correlated with N2O content but negatively correlated with oxygen, suggesting an increase of the N2O produced by Thermoproteota under OMZ expansion. Manuscript Ⅲ studied the spatial distribution and activity of anoxygenic (AP) and oxygenic phototrophs (OP) in the Baltic Sea. A rich diversity of OP and AP was revealed. OP exhibited active photosynthesis, while AP showed no detectable photosynthesis in most stations. Both cyanobacterial and eukaryotic OP preferred higher temperatures and upper water layers. AP did not show a significant hydrochemical preference but tended to coexist with the OP community. Overall, this thesis provide insights of how microbial diversity, diverse groups and functions would respond towards climate change induced OMZ expansion in a broad marine scope.