Prochlorococcus cells rely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation

Dalit Roth-Rosenberg, Dikla Aharonovich, Tal Luzzatto-Knaan, Angela Vogts, Luca Zoccarato, Falk Eigemann, Noam Nago, Hans Peter Grossart, Maren Voss, Daniel Sher

Research output: Contribution to journalArticlepeer-review

Abstract

Many microorganisms produce resting cells with very low metabolic activity that allow them to survive phases of prolonged nutrient or energy stress. In cyano-bacteria and some eukaryotic phytoplankton, the production of resting stages is accom-panied by a loss of photosynthetic pigments, a process termed chlorosis. Here, we show that a chlorosis-like process occurs under multiple stress conditions in axenic laboratory cultures of Prochlorococcus, the dominant phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean biogeochemical cycles. In Prochlo-rococcus strain MIT9313, chlorotic cells show reduced metabolic activity, measured as C and N uptake by Nanoscale secondary ion mass spectrometry (NanoSIMS). However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not regrow under axenic conditions when transferred to new media. Nevertheless, cocultures with a heterotrophic bacterium, Alteromonas macleodii HOT1A3, allowed Prochlorococcus to survive nutrient starvation for months. We propose that reliance on co-occurring heterotrophic bacteria, rather than the ability to survive extended starvation as resting cells, underlies the ecological success of Pro-chlorococcus. IMPORTANCE The ability of microorganisms to withstand long periods of nutrient starvation is key to their survival and success under highly fluctuating conditions that are common in nature. Therefore, one would expect this trait to be prevalent among organisms in the nutrient-poor open ocean. Here, we show that this is not the case for Prochlorococcus, a globally abundant and ecologically important marine cyanobacterium. Instead, Prochlorococcus relies on co-occurring heterotrophic bacteria to survive extended phases of nutrient and light starvation. Our results highlight the power of microbial interactions to drive major biogeochemical cycles in the ocean and elsewhere with consequences at the global scale.

Original languageEnglish
Article numbere01846-20
Pages (from-to)1-13
Number of pages13
JournalmBio
Volume11
Issue number4
DOIs
StatePublished - 2020

Bibliographical note

Funding Information:
This study was supported by grant RGP0020/2016 from the Human Frontiers Science Program (to M.V., H.-P.G., and D.S.) and by grant 1635070/2016532 from the NSF-BSF program in Oceanography (NSFOCE-BSF to D.S.). The NanoSIMS at the Leibnitz-Institute for Baltic Sea research in Warnemuende (IOW), was funded by the German Federal Ministry of Education and Research (BMBF), grant 03F0626A.

Publisher Copyright:
© 2020 Roth-Rosenberg et al.

Keywords

  • Heterotrophic bacteria
  • Microbial interactions
  • NanoSIMS
  • Phytoplankton
  • Picocyanobacteria
  • Resting stages

ASJC Scopus subject areas

  • Microbiology
  • Virology

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