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Regulation of Low and High Nucleic Acid Fluorescent Heterotrophic Prokaryote Subpopulations and Links to Viral-Induced Mortality Within Natural Prokaryote-Virus Communities

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Abstract

Flow cytometric analysis of marine prokaryotes routinely reveals two distinct clusters of heterotrophic cells referred to as high nucleic acid fluorescent (HNA) and low nucleic acid fluorescent (LNA) populations. Evidence suggests that these may represent physiologically and ecologically distinct prokaryote populations. According to the “kill the winner” hypothesis, viral lysis reduces the efficiency of the microbial loop by decreasing the biomass and activity of the most abundant and active members of a population (i.e., competition specialist). Thus, viral-induced mortality may vary according to the physiology of HNA and LNA cells, with implications for the marine carbon cycle. Here, the abundance and production of heterotrophic prokaryotic populations were assessed in the North Atlantic during two phases of the annual plankton cycle and related to bottom-up (i.e., organic carbon variability) and top-down processes (i.e., viral abundance and lytic production). Our results demonstrate that the relative abundance of HNA and LNA heterotrophic cells and heterotrophic prokaryote production vary according to organic carbon variability in the water column, which can be strongly influenced by the physical eddy field (i.e., type of eddy: cyclonic, anticyclonic, or no eddy). In addition, the abundance and lytic production of virus subpopulations were correlated with  the cellular production and abundance of heterotrophic HNA and LNA prokaryote communities. Our data suggest group- and activity-specific linkages between hosts and viruses (i.e., HNA-V1 and LNA-V2). Specifically, V1 had a greater contribution to total viral production (i.e., 2.6-fold higher than V2 viruses), similar to their putative host. Finally, we explore potential implications of group- and activity-specific linkages between host and virus groups on the flux of carbon through the microbial food web.

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Acknowledgments

We thank the captains and crews of the R/V Atlantis for their help with sampling during the cruises. Furthermore, we thank Nerissa Fisher and Nicholas Huynh for their on-board assistance, Peter Gaube and Ali Della-Penna for their useful discussions regarding the physical data and Luis Bolonas and Steve Giovannoni for sharing microbial genomics data. We further acknowledge NSF-1537943 for C. Carlson.

Funding

This research was supported by the National Aeronautics and Space Administration North Atlantic Aerosol and Marine Ecosystems Study (NAAMES; grant NNX15AF30G).

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Authors and Affiliations

  1. Department of Botany and Plant Pathology, Cordley Hall 2082, Oregon State University, Corvallis, OR, 97331-29052, USA

    Kristina D. A. Mojica & Mike J. Behrenfeld

  2. Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA, 93106-6250, USA

    Craig A. Carlson

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  1. Kristina D. A. Mojica
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  2. Craig A. Carlson
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  3. Mike J. Behrenfeld
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Correspondence to Kristina D. A. Mojica.

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Mojica, K.D.A., Carlson, C.A. & Behrenfeld, M.J. Regulation of Low and High Nucleic Acid Fluorescent Heterotrophic Prokaryote Subpopulations and Links to Viral-Induced Mortality Within Natural Prokaryote-Virus Communities. Microb Ecol 79, 213–230 (2020). https://doi.org/10.1007/s00248-019-01393-9

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