In Situ Bacterioplankton Growth Partitioning by High-Resolution Metatranscriptomics

Microbial communities are fundamental to marine trophic webs, elemental cycling and geochemical transformations. Yet we lack high phylogenetic resolution measurements or good indicators of how fast different taxa are actively growing in situ. Here, we use high temporal resolution transcriptomics to phylogenetically disentangle an index of growth before and after a short spring phytoplankton bloom, by quantifying the phylogenetic distribution of the expression of ftsZ, a gene encoding for a protein involved in cell division. We interpret the relative abundances of ftsZ transcripts as a general indicator of how growth was distributed amongst taxa. This expression was also compared to RNase P to estimate how each organism's transcriptional resources were allocated to replication versus other functions. During the time-series, we observed two distinct profiles: prior to and several days after the bloom, ftsZ expression was dominated by Synechococcales, Pelagibacterales and picoeukaryotes, and by Rhodobacterales, SAR92 and SAR86 as the bloom declined. Whilst similar successional patterns have been observed previously, our dataset extends these observations by resolving transcriptional and replication-associated activity at high temporal resolution, enabling the detection of disproportionate contributions during bloom development and turnover. Our approach is scalable and will inform conceptual and mechanistic models of planktonic food webs.