Single-cell mass accumulation reveals bacterioplankton growth rate in native seawater

Abstract

AO_SCPLOWBSTRACTC_SCPLOWThe growth of marine microbial communities drives biogeochemical cycling of carbon and other elements, yet the growth rates of individual species within complex ocean ecosystems remain poorly understood. In particular, the coexistence of a large diversity of copiotrophic bacteria, which are capable of fast growth but typically remain at low abundance, has been interpreted as a feast or famine existence. Here we show that contrary to the notion of infrequent growth, Vibrio bacteria exhibited consistent growth rates in coastal ocean samples, despite representing only a small fraction of the total community. These observations were enabled by a suspended microchannel resonator (SMR), which we adapted to function as a single-cell chemostat. By maintaining a continuous supply of native seawater around each trapped cell, we prevented nutrient depletion and used the SMRs high mass precision to resolve growth rates that are otherwise undetectable. Vibrio species displayed significantly larger cell mass and faster growth than other community members across samples collected at different temporal intervals from days to years. Surprisingly, their growth was consistently limited by carbon, contrary to the expectation that heterotrophic bacteria in the euphotic zone would be limited by nitrogen and phosphorus due to competition with algae. The correlation between cell mass and growth rate of Vibrionaceae in seawater followed established growth laws derived from laboratory conditions, suggesting that growth physiology observed in pure cultures is applicable to wild bacterial populations. Overall, our findings suggest that rare species may play a disproportionately large role in the marine carbon cycle, with rapid biomass turnover driven by a combination of high growth rates balanced by intense predation.