Highly enriched N-containing organic molecules of Synechococcus lysates and their rapid transformation by heterotrophic bacteria

Abstract

Phytoplankton are major contributors of labile dissolved organic matter to marine euphotic zone ecosystems. Viral-mediated phytoplankton lysis releases a considerable amount of bioavailable cellular contents and facilitates localized heterotrophic bacterial growth. The rapid turnover times of this labile organic matter renders it difficult to trace their transformation within natural environments. In the present study, we used a model phototroph-heterotroph coculture system to investigate the organic molecular variation during cyanophage-induced Synechococcus lysis and post-lysis periods using fluorescence spectroscopy and ultrahigh resolution mass spectrometry analyses. Approximately 80% of the Synechococcus lysates were respired to carbon dioxide within 2 days coupled to rapid regeneration of inorganic nutrients. Five fluorescent dissolved organic matter components were detected in the incubations including four humic-like and one protein-like components, and their abundances varied markedly with the succession of the viral lysis process. Viral lysis promoted the transformation of Synechococcus biomass to dissolved organic matter, and heterotrophic bacterial metabolism facilitated the transformation of organic molecules from relatively high (avg. ~ 430 Da) to low (avg. ~ 360 Da) molecular weight, corresponding to variation in their bioavailability. The Synechococcus-derived organic matter was highly enriched in N-containing organic molecules. Identified metabolites within the cultures primarily comprised amino acids or oligopeptides and other low-molecular-weight organic acids, carbohydrates, nucleotides, lipids, biogenic amines, and porphyrins. Among these, oligopeptides, nucleotides, and lipid compounds significantly increased with viral lysis. These results provide insight into biogeochemical cycling mediated by viral shunts in oceans, thus deepening our understanding of microbial food webs at the molecular level.