Redox-controlled restructuring of marine microbial ecosystems during oceanic anoxic events

Abstract

During the Phanerozoic, the ocean repeatedly experienced periods of widespread deoxygenation known as oceanic anoxic events. Geological records from these events indicate a profound shift in marine microbial ecosystems. While cyanobacterial biomarkers are found broadly, those of anoxygenic photosynthetic green sulfur bacteria are restricted to upwelling regions or topographic highs. However, the quantitative mechanisms triggering this transition and the spatial heterogeneity of primary producers remain ambiguous. Here, using a new high-resolution one-dimensional ocean biogeochemical model explicitly incorporating a marine microbial ecosystem, we systematically evaluated the global effects of increases in riverine phosphorus input rates and sea surface temperature. We show that phosphorus-driven eutrophication and ocean warming-induced reductions in both O2 solubility and export efficiency result in surface ocean deoxygenation, leading to the restructuring of the marine microbial ecosystem. The emergence of anoxic water masses enhances denitrification and establishes a nitrogen-depleted environment, promoting the proliferation of N2-fixing cyanobacteria. With further deoxygenation, euxinic water masses develop within the photic zone, allowing green sulfur bacteria to thrive below the redoxcline, resulting in a vertical ecological segregation with oxygenic photoautotrophs and N2-fixing cyanobacteria. Moreover, an abundant supply of nutrients and H2S in upwelling regions causes more severe deoxygenation within the photic zone than in the open ocean, providing a niche suitable for green sulfur bacteria and driving a more drastic restructuring of primary producers. These findings elucidate the quantitative impacts of global climate perturbations and regional upwelling on the surface ocean, offering crucial insights into how surface ocean biogeochemistry and marine microbial ecosystems fluctuated during oceanic anoxic events.