Human activities-impacted lake dissolved organic matter (DOM) affects phycosphere microbial diversity and DOM diversification via carbon metabolism

Abstract

Photosynthetic carbon sequestration and microbial carbon metabolism are major processes of algae-bacteria interactions, affecting pollutant degradation as well as fundamental biogeochemical cycles in aquatic systems. Human-induced land-use changes greatly alter the molecular composition and input of terrestrial dissolved organic matter (DOM) in inland lakes. However, how the origin of DOM leads to varying effects on phycosphere microbial communities or molecular composition of DOM, e.g., via carbon metabolism, has been little studied in freshwater. Here, we incubated the cyanobacterium Microcystis aeruginosa and a bacterial community from natural lakes to establish an alga-bacteria model system. This allowed us to investigate how DOM from different sources affects phycosphere microbial diversity and DOM diversification. We showed that Suwannee River fulvic acid (SRFA), Suwannee River natural organic matter (SRNOM) and cropland lake DOM promote algal growth, whereas DOM from an urban lake inhibits algal growth. Algal metabolites and DOM together shaped the chemotaxis response of phycosphere communities. High-resolution mass spectrometry analysis demonstrated that DOM chemo-diversity tended to become uniform after interactions of diverse DOM sources with the algae-bacteria symbiosis system. Molecular thermodynamic analysis of DOM based on a substrate-explicit model further verified that microbial interactions render DOM less bioavailable and thus increase recalcitrant DOM formation. Metabolome analysis uncovered that DOM addition intensifies metabolic pathways related to labile and recalcitrant DOM utilization (mainly lignin/carboxyl-rich alicyclic molecule (CRAM)-like DOM, unsaturated hydrocarbon), whereby cofactor and vitamin metabolism represented an extremely strong activity in all metabolic pathways. Our results highlight covariation and interactions of DOM with microbial metabolism at the molecular level and expands our understanding of microbially mediated DOM shaping aquatic carbon cycling.