Abstract
Coral reefs are declining globally as their primary producer communities shift from stony coral to fleshy macroalgae dominance. Previously, we have shown that the rise of fleshy macroalgae produces dissolved organic carbon (DOC) that lead to microbialization and coral death. Here we test the hypothesis that the biophysical cause of bacterial biomass accumulation is a relative decrease in electron acceptors relative to electron donors due to O2 loss from macroalgae. We show that 37 % of photosynthetic O2 produced by reef fleshy macroalgae is lost in the form of gas through ebullition from algae surfaces. O2 loss increases DOC:O2 ratios, decoupling the photosynthetically fixed carbon from oxidative potential for respiration. This biogeochemical environment drives heterotrophic microbes to increase cell-specific DOC consumption and cell sizes, accumulating biomass. In contrast, corals do not lose oxygen and support the growth of smaller and fewer bacteria. In situ biomass and metagenomic analyses of 87 reefs across the Pacific and Caribbean show that on algae-dominated reefs bacteria accumulate organic carbon through a Warburg-like increase in aerobic glycolytic metabolism. Because of its biophysical basis, microbialization is predicted to occur in other marine ecosystems shifting primary producer assemblages, such as planktonic communities in warming and acidifying conditions.
Footnotes
Statement of authorship: CBS, BR, LWK, MH, MV, YT, AH and FR designed experiments and sampling; CBS, TR, HV, BR, ERP, AL, MV, and AH performed experiments; CBS, TR, AB, TL, and SM generated microscopy and metagenomic data; CBS and BB performed statistical analyses; CS wrote the manuscript and all authors contributed substantially with revisions.
Data availability Statement Experimental data are provided as supporting datasets and in FigShare (https://doi.org/10.6084/m9.figshare.7170254.v1). Metagenomic data are available in the NCBI SRA under PRJNA494971.
