Abstract

Estimation of prokaryotic growth rates is critical to understand the ecological role and contribution of different microbes to marine biogeochemical cycles. However, there is a general lack of knowledge on what factors control the growth rates of different prokaryotic groups and how these vary between sites and along seasons at a given site. We carried out several manipulation experiments during the four astronomical seasons in the coastal NW Mediterranean in order to evaluate the impact of grazing, viral mortality, resource competition and light on the growth and loss rates of prokaryotes. Gross and net growth rates of different bacterioplankton groups targeted by group-specific CARD-FISH probes and infrared microscopy (for aerobic anoxygenic phototrophs, AAP), were calculated from changes in cell abundances. Maximal group-specific growth rates were achieved when both predation pressure and nutrient limitation were experimentally minimized, while only a minimal effect of viral pressure on growth rates was observed; nevertheless, the response to predation removal was more remarkable in winter, when the bacterial community was not subjected to nutrient limitation. Although all groups showed increases in their growth rates when resource competition as well as grazers and viral pressure were reduced, Alteromonadaceae consistently presented the highest rates in all seasons. The response to light availability was generally weaker than that to the other factors, but it was variable between seasons. In summer and spring, the growth rates of AAP were stimulated by light whereas the growth of the SAR11 clade (likely containing proteorhodopsin) was enhanced by light in all seasons. Overall, our results set thresholds on bacterioplankton group-specific growth and mortality rates and contribute to estimate the seasonally changing contribution of various bacterioplankton groups to the function of microbial communities. Our results also indicate that the least abundant groups display the highest growth rates, contributing to the recycling of organic matter to a much greater extent than what their abundances alone would predict.

Highlights

  • Growth rates, along with the rates of mortality, determine the biomass levels of bulk bacterioplankton communities and of specific taxonomic groups, and set the contribution of microorganisms to ocean biogeochemical cycles

  • Some previous studies have put the focus on the importance of these factors in determining the net and gross growth rates of different bacterioplankton ­groups[4,5,9,39,40], but most of these studies were restricted to specific short time periods, and, as far as we know, only two of them looked at the factors controlling bacterial growth rates along longer time scales in a coastal upwelling ­system[3] or an ­estuary[39], but none in an oligotrophic system

  • The abundances of heterotrophic nanoflagellates were fairly similar among seasons, while the viral abundance was low in spring and reached the highest value in fall

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Summary

Introduction

Along with the rates of mortality, determine the biomass levels of bulk bacterioplankton communities and of specific taxonomic groups, and set the contribution of microorganisms to ocean biogeochemical cycles (see review by ­Kirchman[1]). Variability of nutrient concentrations and bacterioplankton nutrient limitation along seasons has been ­described[34,35,36,37,38] Despite this wealth of studies, information about seasonal changes in the bottom-up and top-down controls on bacterial growth rates is scarce. To evaluate the impact of top-down (protists and viruses) and bottom-up (resources) controls on bacterial growth rates under different light conditions, we conducted manipulation experiments during the four astronomical seasons and determined the net and gross growth rates of different CARD-FISH-determined bacterioplankton groups at the Blanes Bay Microbial Observatory (BBMO), an oligotrophic coastal site in the Northwest Mediterranean. The results contribute to our knowledge of the magnitude of marine prokaryotic growth rates and the role that top-down and bottom-up pressures, as well as light, play in controlling them over a seasonal cycle

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