Growth rates of marine prokaryotes are extremely diverse, even among closely related taxa

Ona Deulofeu-Capo; Marta Sebastián; Adrià Auladell; Clara Cardelús; Isabel Ferrera; Olga Sánchez; Josep M Gasol

doi:10.1093/ismeco/ycae066

Growth rates of marine prokaryotes are extremely diverse, even among closely related taxa

ISME Commun. 2024 May 2;4(1):ycae066. doi: 10.1093/ismeco/ycae066. eCollection 2024 Jan.

Authors

Ona Deulofeu-Capo¹, Marta Sebastián¹, Adrià Auladell², Clara Cardelús¹, Isabel Ferrera³, Olga Sánchez⁴, Josep M Gasol¹

Affiliations

¹ Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Barcelona, Catalunya 08003, Spain.
² Institut de Biologia Evolutiva, CSIC-UPF, Barcelona 08003, Catalunya, Spain.
³ Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, IEO-CSIC, Puerto Pesquero s/n, Fuengirola 29640, Málaga, Spain.
⁴ Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra, Catalunya 08193, Spain.

Abstract

Marine prokaryotes play crucial roles in ocean biogeochemical cycles, being their contribution strongly influenced by their growth rates. Hence, elucidating the variability and phylogenetic imprint of marine prokaryotes' growth rates are crucial for better determining the role of individual taxa in biogeochemical cycles. Here, we estimated prokaryotic growth rates at high phylogenetic resolution in manipulation experiments using water from the northwestern Mediterranean Sea. Experiments were run in the four seasons with different treatments that reduced growth limiting factors: predators, nutrient availability, viruses, and light. Single-amplicon sequence variants (ASVs)-based growth rates were calculated from changes in estimated absolute abundances using total prokaryotic abundance and the proportion of each individual ASV. The trends obtained for growth rates in the different experiments were consistent with other estimates based on total cell-counts, catalyzed reporter deposition fluorescence in situ hybridization subcommunity cell-counts or metagenomic-operational taxonomic units (OTUs). Our calculations unveil a broad range of growth rates (0.3-10 d^-1) with significant variability even within closely related ASVs. Likewise, the impact of growth limiting factors changed over the year for individual ASVs. High numbers of responsive ASVs were shared between winter and spring seasons, as well as throughout the year in the treatments with reduced nutrient limitation and viral pressure. The most responsive ASVs were rare in the in situ communities, comprising a large pool of taxa with the potential to rapidly respond to environmental changes. Essentially, our results highlight the lack of phylogenetic coherence in the range of growth rates observed, and differential responses to the various limiting factors, even for closely related taxa.

Keywords: amplicon metabarcoding; growth rate; manipulation experiment; marine prokaryotes.