Distinct microbial response to organic matter from nitrogen-starved and virus-infected phytoplankton

Abstract

When phytoplankton die they release dissolved organic matter (DOM) that feeds co-occurring heterotrophic bacteria. We show that death due to phage infection and nitrogen starvation result in different changes to the macromolecular structure of Prochlorococcus, a globally abundant cyanobacterium, and that the resulting DOM elicits different microbial responses. Viral infection led to increased RNA and DNA content in Prochlorococcus whereas nitrogen starvation led to a lower protein content. DOM released from phage-infected cells induced high secondary (bacterial) production, while DOM from starved cells increased dark (heterotrophic) primary production in natural microbial communities from the oligotrophic Eastern Mediterranean Sea. Through 16S and 18S amplicon sequencing, metagenomics, and laboratory experiments we identify Alteromonadaceae and Rhodobacteraceae as heterotrophic taxa responding differently to the two DOM sources. We propose that distinct forms of phytoplankton mortality drive shifts in microbial community metabolism, including differential activity of pathways for heterotrophic carbon fixation, likely through anaplerotic reactions.