Vitamin B12 release through bacteriophage-mediated cell lysis of the marine bacterium Sulfitobacter sp. M39

Sabiha Sultana; Stefan Bruns; Armando Pacheco-Valenciana; Maliheh Mehrshad; Heinz Wilkes; Meinhard Simon; Sarahi Garcia; Gerrit Wienhausen

doi:10.1093/ismeco/ycaf136

Vitamin B₁₂ release through bacteriophage-mediated cell lysis of the marine bacterium Sulfitobacter sp. M39

ISME Commun. 2025 Aug 29;5(1):ycaf136. doi: 10.1093/ismeco/ycaf136. eCollection 2025 Jan.

Authors

Sabiha Sultana¹, Stefan Bruns¹, Armando Pacheco-Valenciana², Maliheh Mehrshad³, Heinz Wilkes¹, Meinhard Simon^{1

4}, Sarahi Garcia^{1

2

4}, Gerrit Wienhausen¹

Affiliations

¹ Institute for Chemistry and Biology of the Marine Environment (ICBM), School of Mathematics and Science, Carl von Ossietzky Universität Oldenburg, Oldenburg, Germany.
² Department of Ecology, Environment, and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden.
³ Department of Aquatic Sciences and Assessment, Science for Life Laboratory, Swedish University of Agricultural Sciences, Uppsala, Sweden.
⁴ Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg (HIFMB), Oldenburg, Germany.

Abstract

Vitamin B₁₂ (B₁₂) is an essential cofactor for vital metabolic processes in both prokaryotes and eukaryotes. De novo B₁₂ biosynthesis is exclusively carried out by a modicum of prokaryotes, although being required by most organisms. Recently, it has been demonstrated that not all B₁₂-prototrophic bacteria voluntarily share this vital cofactor and, therefore, are termed B₁₂-retainers. Consequently, low biosynthesis potential and limited voluntary release lead to a large discrepancy between availability and demand for B₁₂ in the ocean, indicating that release of B₁₂ may be an important control. Hence, in this study, we examined a specific release process, cell lysis after phage infection. We isolated bacteriophages specific for the B₁₂-prototrophic, yet B₁₂-retainer bacterium Sulfitobacter sp. M39. The addition of the bacteriophages to a Sulfitobacter sp. M39 mono-culture led to a significant increase in virus-like particles, reduced bacterial growth, and quantifiable extracellular dissolved B₁₂. When introducing bacteriophages to a co-culture comprising the host bacterium and the B₁₂-auxotrophic diatom Thalassiosira pseudonana, we observed rapid response in the form of microalgal growth. Our results indicate that B₁₂ is released as a result of bacteriophage-mediated cell lysis of Sulfitobacter sp. M39, enabling the growth of T. pseudonana in co-culture and possibly other microbes in nature. Therefore, we propose that bacteriophage-mediated cell lysis is a key mechanism for the release of essential metabolites, including vitamins, and given the estimated bacteriophage infection rates in the ocean, it plays a crucial role in the B-vitamin cycle in the marine environment.

Keywords: bacteriophage-mediated cell lysis; bacteriophages; cobalamin; diatom; marine microbial community; metabolite cross-feeding; microbial interaction; vitamin B12.