PMID- 37195198 OWN - NLM STAT- MEDLINE DCOM- 20230703 LR - 20240123 IS - 2379-5077 (Electronic) IS - 2379-5077 (Linking) VI - 8 IP - 3 DP - 2023 Jun 29 TI - In situ cell division and mortality rates of SAR11, SAR86, Bacteroidetes, and Aurantivirga during phytoplankton blooms reveal differences in population controls. PG - e0128722 LID - 10.1128/msystems.01287-22 [doi] LID - e01287-22 AB - Net growth of microbial populations, that is, changes in abundances over time, can be studied using 16S rRNA fluorescence in situ hybridization (FISH). However, this approach does not differentiate between mortality and cell division rates. We used FISH-based image cytometry in combination with dilution culture experiments to study net growth, cell division, and mortality rates of four bacterial taxa over two distinct phytoplankton blooms: the oligotrophs SAR11 and SAR86, and the copiotrophic phylum Bacteroidetes, and its genus Aurantivirga. Cell volumes, ribosome content, and frequency of dividing cells (FDC) co-varied over time. Among the three, FDC was the most suitable predictor to calculate cell division rates for the selected taxa. The FDC-derived cell division rates for SAR86 of up to 0.8/day and Aurantivirga of up to 1.9/day differed, as expected for oligotrophs and copiotrophs. Surprisingly, SAR11 also reached high cell division rates of up to 1.9/day, even before the onset of phytoplankton blooms. For all four taxonomic groups, the abundance-derived net growth (-0.6 to 0.5/day) was about an order of magnitude lower than the cell division rates. Consequently, mortality rates were comparably high to cell division rates, indicating that about 90% of bacterial production is recycled without apparent time lag within 1 day. Our study shows that determining taxon-specific cell division rates complements omics-based tools and provides unprecedented clues on individual bacterial growth strategies including bottom-up and top-down controls. IMPORTANCE The growth of a microbial population is often calculated from their numerical abundance over time. However, this does not take cell division and mortality rates into account, which are important for deriving ecological processes like bottom-up and top-down control. In this study, we determined growth by numerical abundance and calibrated microscopy-based methods to determine the frequency of dividing cells and subsequently calculate taxon-specific cell division rates in situ. The cell division and mortality rates of two oligotrophic (SAR11 and SAR86) and two copiotrophic (Bacteroidetes and Aurantivirga) taxa during two spring phytoplankton blooms showed a tight coupling for all four taxa throughout the blooms without any temporal offset. Unexpectedly, SAR11 showed high cell division rates days before the bloom while cell abundances remained constant, which is indicative of strong top-down control. Microscopy remains the method of choice to understand ecological processes like top-down and bottom-up control on a cellular level. FAU - Bruwer, Jan D AU - Bruwer JD AUID- ORCID: 0000-0002-7317-4613 AD - Max Planck Institute for Marine Microbiology , Bremen, Germany. FAU - Orellana, Luis H AU - Orellana LH AUID- ORCID: 0000-0002-2766-5243 AD - Max Planck Institute for Marine Microbiology , Bremen, Germany. FAU - Sidhu, Chandni AU - Sidhu C AUID- ORCID: 0000-0003-1386-1881 AD - Max Planck Institute for Marine Microbiology , Bremen, Germany. FAU - Klip, Helena C L AU - Klip HCL AUID- ORCID: 0000-0002-0699-3934 AD - Alfred-Wegener-Institut, Helmholtz-Zentrum fur Polar- und Meeresforschung, Biologische Anstalt Helgoland , Helgoland, Germany. FAU - Meunier, Cedric L AU - Meunier CL AUID- ORCID: 0000-0002-4070-4286 AD - Alfred-Wegener-Institut, Helmholtz-Zentrum fur Polar- und Meeresforschung, Biologische Anstalt Helgoland , Helgoland, Germany. FAU - Boersma, Maarten AU - Boersma M AUID- ORCID: 0000-0003-1010-026X AD - Alfred-Wegener-Institut, Helmholtz-Zentrum fur Polar- und Meeresforschung, Biologische Anstalt Helgoland , Helgoland, Germany. AD - University of Bremen , Bremen, Germany. FAU - Wiltshire, Karen H AU - Wiltshire KH AUID- ORCID: 0000-0002-7148-0529 AD - Alfred-Wegener-Institut, Helmholtz-Zentrum fur Polar- und Meeresforschung, Biologische Anstalt Helgoland , Helgoland, Germany. AD - Alfred-Wegener-Institut, Helmholtz-Zentrum fur Polar- und Meeresforschung, Wattenmeerstation, List auf Sylt , Bremerhaven, Germany. FAU - Amann, Rudolf AU - Amann R AUID- ORCID: 0000-0002-0846-7372 AD - Max Planck Institute for Marine Microbiology , Bremen, Germany. FAU - Fuchs, Bernhard M AU - Fuchs BM AUID- ORCID: 0000-0001-9828-1290 AD - Max Planck Institute for Marine Microbiology , Bremen, Germany. LA - eng GR - Max Planck Society/ GR - FU 627/2-2/Deutsche Forschungsgemeinschaft (DFG)/ GR - AM 73/9-2/Deutsche Forschungsgemeinschaft (DFG)/ PT - Journal Article DEP - 20230517 PL - United States TA - mSystems JT - mSystems JID - 101680636 RN - 0 (RNA, Ribosomal, 16S) SB - IM EIN - mSystems. 2024 Jan 23;9(1):e0119623. PMID: 38117073 MH - *Bacteroidetes/genetics MH - *Phytoplankton/genetics MH - RNA, Ribosomal, 16S/genetics MH - In Situ Hybridization, Fluorescence MH - Population Control MH - Seawater/microbiology MH - Bacteria MH - Cell Division PMC - PMC10308942 OTO - NOTNLM OT - cell division OT - copiotrophy OT - growth OT - image cytometry OT - mortality OT - oligotrophy OT - spring bloom COIS- The authors declare no conflict of interest. EDAT- 2023/05/17 13:10 MHDA- 2023/07/03 06:41 PMCR- 2023/05/17 CRDT- 2023/05/17 10:04 PHST- 2023/07/03 06:41 [medline] PHST- 2023/05/17 13:10 [pubmed] PHST- 2023/05/17 10:04 [entrez] PHST- 2023/05/17 00:00 [pmc-release] AID - 01287-22 [pii] AID - msystems.01287-22 [pii] AID - 10.1128/msystems.01287-22 [doi] PST - ppublish SO - mSystems. 2023 Jun 29;8(3):e0128722. doi: 10.1128/msystems.01287-22. Epub 2023 May 17.