Acclimation temperature influences phage susceptibility in a toxin-producing strain of Microcystis aeruginosa

Kennedi Hambrick, Laura Smith, Robbie Martin, Bofan Wei, Raunak Dey, Gregory Boyer, Joshua Weitz, David Talmy, Steven Wilhelm, Erik Zinser (2026) Acclimation temperature influences phage susceptibility in a toxin-producing strain of Microcystis aeruginosa Microbiol Spectr (IF: 4.1) e0337925

Abstract

Microcystis aeruginosa is a freshwater cyanobacterium known for its role in the formation of harmful algal blooms. However, less well characterized are the host-phage interactions that occur in these toxic blooms. Here, we describe the relationship between a microcystin-producing strain of M. aeruginosa, NIES-298, and a lytic bacteriophage Ma-LMM01. In this study, we explored how host pre-acclimation to different temperature conditions influenced sensitivity to subsequent infection by Ma-LMM01. We focused on 19°C, a cooler temperature often associated with microcystin-producing blooms in spring/early summer, and 26°C, a warmer temperature often associated with non-microcystin-producing blooms of late summer. M. aeruginosa cultures pre-acclimated to 26°C were completely lysed whether infection occurred at 26°C or 19°C. In contrast, 19°C-acclimated M. aeruginosa grew and resisted infection regardless of infection temperature. We next formulated a mathematical model to investigate the key parameters driving these temperature dynamics. Our modeling suggested both 19°C- and 26°C-acclimated hosts contain resistant subpopulations of comparable abundance but with different degrees of resistance. Specifically, we found the 19°C-acclimated host subpopulation was substantially more resistant to phage infection than the 26°C-acclimated host subpopulation, which was only partially resistant. Overall, our observations demonstrate that M. aeruginosa NIES-298 acclimation to 19°C played a role in the development of resistance to cyanophage Ma-LMM01. These findings suggest new directions to explore the link between physiological changes and infection outcomes for microcystin-producing cyanobacteria in changing environments.IMPORTANCEHarmful cyanobacterial blooms frequently develop in aquatic systems, causing significant ecological and commercial impact, motivating research into factors influencing bloom formation, persistence, and toxicity. Prior studies identified several contributors to the "life cycle" of a toxic bloom, including abiotic influences, community structure, and host-viral interactions. This paper explores two of these factors, temperature and viral-host interactions, on the growth and survival of Microcystis aeruginosa NIES-298. We report the first observation that the acclimation temperature of M. aeruginosa influences phage susceptibility, and through mathematical modeling, explore resistant subpopulation dynamics. We observed that cells acclimated to cold temperatures, such as those experienced in spring/early summer, were resistant to phage, while those acclimated to warmer temperatures, such as those experienced in late summer, were not. This work contributes to the fields of freshwater ecology and microbial physiology by advancing our understanding of the interplay between host-phage interactions and abiotic influences in toxic algal bloom formation.

Links

http://www.ncbi.nlm.nih.gov/pubmed/42294697
http://dx.doi.org/10.1128/spectrum.03379-25

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