The hidden seasonality of the rare biosphere in coastal marine bacterioplankton

Abstract

Rare microbial taxa are increasingly recognized to play key ecological roles, but knowledge of their spatio-temporal dynamics is lacking. In a time-series study in coastal waters, we detected 83 bacterial lineages with significant seasonality, including environmentally relevant taxa where little ecological information was available. For example, Verrucomicrobia had recurrent maxima in summer, while the Flavobacteria NS4, NS5 and NS2b clades had contrasting seasonal niches. Among the seasonal taxa, only 4 were abundant and persistent, 20 cycled between rare and abundant and, remarkably, most of them (59) were always rare (contributing < 1% of total reads). We thus demonstrate that seasonal patterns in marine bacterioplankton are largely driven by lineages that never sustain abundant populations. A fewer number of rare taxa (20) also produced episodic 'blooms', and these events were highly synchronized, mostly occurring on a single month. The recurrent seasonal growth and loss of rare bacteria opens new perspectives on the temporal dynamics of the rare biosphere, hitherto mainly characterized by dormancy and episodes of 'boom and bust', as envisioned by the seed-bank hypothesis. The predictable patterns of seasonal reoccurrence are relevant for understanding the ecology of rare bacteria, which may include key players for the functioning of marine ecosystems.