期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：36
DOI：10.1073/pnas.2203057119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Microbial growth is often limited by key nutrients like phosphorus (P) across the global ocean. A major response to P limitation is the replacement of membrane phospholipids with non-P lipids to reduce their cellular P quota. However, the biological “costs” of lipid remodeling are largely unknown. Here, we uncover a predator–prey interaction trade-off whereby a lipid-remodeled bacterial prey cell becomes more susceptible to digestion by a protozoan predator facilitating its rapid growth. Thus, we highlight a complex interplay between adaptation to the abiotic environment and consequences for biotic interactions (grazing), which may have important implications for the stability and structuring of microbial communities and the performance of the marine food web.
Phosphorus (P) is a key nutrient limiting bacterial growth and primary production in the oceans. Unsurprisingly, marine microbes have evolved sophisticated strategies to adapt to P limitation, one of which involves the remodeling of membrane lipids by replacing phospholipids with non-P-containing surrogate lipids. This strategy is adopted by both cosmopolitan marine phytoplankton and heterotrophic bacteria and serves to reduce the cellular P quota. However, little, if anything, is known of the biological consequences of lipid remodeling. Here, using the marine bacterium
Phaeobacter sp. MED193 and the ciliate
Uronema marinum as a model, we sought to assess the effect of remodeling on bacteria–protist interactions. We discovered an important trade-off between either escape from ingestion or resistance to digestion. Thus,
Phaeobacter grown under P-replete conditions was readily ingested by
Uronema, but not easily digested, supporting only limited predator growth. In contrast, following membrane lipid remodeling in response to P depletion,
Phaeobacter was less likely to be captured by
Uronema, thanks to the reduced expression of mannosylated glycoconjugates. However, once ingested, membrane-remodeled cells were unable to prevent phagosome acidification, became more susceptible to digestion, and, as such, allowed rapid growth of the ciliate predator. This trade-off between adapting to a P-limited environment and susceptibility to protist grazing suggests the more efficient removal of low-P prey that potentially has important implications for the functioning of the marine microbial food web in terms of trophic energy transfer and nutrient export efficiency.
