Microbial transformation of virus-induced dissolved organic matter from picocyanobacteria: coupling of bacterial diversity and DOM chemodiversity

Abstract

Picocyanobacteria make up half of the ocean’s primary production, and they are subjected to frequent viral infection. Viral lysis of picocyanobacteria is a major driving force converting biologically fixed carbon into dissolved organic carbon (DOC). Viral-induced dissolved organic matter (vDOM) released from picocyanobacteria provides complex organic matter to bacterioplankton in the marine ecosystem. In order to understand how picocyanobacterial vDOM are transformed by bacteria and the impact of this process on bacterial community structure, viral lysate of picocyanobacteria was incubated with coastal seawater for 90 days. The transformation of vDOM was analyzed by ultrahigh-resolution mass spectrometry and the shift of bacterial populations analyzed using high-throughput sequencing technology. Addition of picocyanobacterial vDOM introduced abundant nitrogen components into the coastal water, which were largely degraded during the 90 days’ incubation period. However, some DOM signatures were accumulated and the total assigned formulae number increased over time. In contrast to the control (no addition of vDOM), bacterial community enriched with vDOM changed markedly with increased biodiversity indices. The network analysis showed that key bacterial species formed complex relationship with vDOM components, suggesting the potential correspondence between bacterial populations and DOM molecules. We demonstrate that coastal bacterioplankton are able to quickly utilize and transform lysis products of picocyanobacteria, meanwhile, bacterial community varies with changing chemodiverisity of DOM. vDOM released from picocyanobacteria generated a complex labile DOM pool, which was converted to a rather stable DOM pool after microbial processing in the time frame of days to weeks.

Impact of Viral Lysis on the Composition of Bacterial Communities and Dissolved Organic Matter in Deep-Sea Sediments

“…This is in accordance with other studies, showing that labile lysis products and virus particles were quickly metabolized, providing organic compounds and key elements to heterotrophic microorganisms [5,19,78]. In contrast to previous observations, N-containing compounds rather increased during the experiment [12]. The degradation of these molecules might have been masked by a constant input of amino acids and peptides due to leaching from the slurries.…”

“…The decomposition of bulk organic compounds and molecules that were probably liberated by slurrying led to a gradual removal of bio-available components, accompanied by a relative accumulation of more refractory compounds [66,70]. Despite the clear alteration of the DOM composition by the slurry process, DOM analysis revealed that prophage induction had modified the chemical composition and character of the benthic DOM pool, which is in line with previous studies [12,20,71]. During virus-mediated cell lysis, the chemical complexity of DOM increased and resulted in the generation of compounds that were compositionally distinct from the bulk DOM.…”

“…The induction can happen spontaneously [10] or by physical stress and chemical inducing agents [11]. The virus-mediated generation of dissolved organic matter (vDOM) provides substrates for indigenous prokaryotes [12] and represents a shortcut in the marine foodweb, the so-called "viral shunt" [7]. It is estimated that viral lysis accounts for the annual release of up to 0.63 Gt of organic carbon in marine sediments [4].…”

Synechococcus sp. Strain PCC7002 Uses Sulfide:Quinone Oxidoreductase To Detoxify Exogenous Sulfide and To Convert Endogenous Sulfide to Cellular Sulfane Sulfur

“…Cyanobacteria possess both photosynthesis system I (PSI) and photosynthesis system II (PSII), and they usually perform oxygenic photosynthesis but can do anoxygenic photosynthesis (41,42). They are effective participants in marine carbon cycles (43). Cyanobacteria are found to inhabit multiple marine habitats, and Synechococcus spp.…”

Minireview: The role of viruses in marine photosynthetic biofilms

“…In addition to molecular approaches, some advanced chemical methods have been applied to virus-bacteria and virus-algae interactions in the marine environments. These include ultraviolet-visible absorbance, excitation emission matrix fluorescence, ultrahigh-resolution mass spectrometry and nuclear magnetic resonance spectroscopy (Zhao et al 2017(Zhao et al , 2019. The applications of these methods to photosynthetic biofilms will also significantly improve our understanding of the interactions between virus, bacteria and algae in the future.…”