Ecological dynamics and co-occurrence among marine phytoplankton, bacteria and myoviruses shows microdiversity matters.

Abstract

Numerous ecological processes, such as bacteriophage infection and phytoplankton-bacterial interactions, often occur via strain-specific mechanisms. Therefore, studying the causes of microbial dynamics should benefit from highly resolving taxonomic characterizations. We sampled daily to weekly over 5 months following a phytoplankton bloom off Southern California and examined the extent of microdiversity, that is, significant variation within 99% sequence similarity clusters, operational taxonomic units (OTUs), of bacteria, archaea, phytoplankton chloroplasts (all via 16S or intergenic spacer (ITS) sequences) and T4-like-myoviruses (via g23 major capsid protein gene sequence). The extent of microdiversity varied between genes (ITS most, g23 least) and only temporally common taxa were highly microdiverse. Overall, 60% of taxa exhibited microdiversity; 59% of these had subtypes that changed significantly as a proportion of the parent taxon, indicating ecologically distinct taxa. Pairwise correlations between prokaryotes and myoviruses or phytoplankton (for example, highly microdiverse Chrysochromulina sp.) improved when using single-base variants. Correlations between myoviruses and SAR11 increased in number (172 vs 9, Spearman>0.65) and became stronger (0.61 vs 0.58, t-test: P<0.001) when using SAR11 ITS single-base variants vs OTUs. Whole-community correlation between SAR11 and myoviruses was much improved when using ITS single-base variants vs OTUs, with Mantel rho=0.49 vs 0.27; these results are consistent with strain-specific interactions. Mantel correlations suggested >1 μm (attached/large) prokaryotes are a major myovirus source. Consideration of microdiversity improved observation of apparent host and virus networks, and provided insights into the ecological and evolutionary factors influencing the success of lineages, with important implications to ecosystem resilience and microbial function.