Trade-offs of lipid remodeling in a marine predator–prey interaction in response to phosphorus limitation

Abstract

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.

Aminolipids elicit functional trade-offs between competitiveness and bacteriophage attachment in Ruegeria pomeroyi

“…A similar phenomenon was shown previously in a bacteria-protist grazer scenario. Bacteria which undergo PlcP-mediated lipid remodelling in response to low phosphorus were less likely to be captured by grazers but became more susceptible to digestion once captured [ 29 ]. Similarly, it appears aminolipid formation, which is independent of the PlcP-mediated lipid remodelling pathway, confers a competitive advantage in the form of nutrient uptake, but exerts trade-offs by rendering the cell more prone to bacteriophage infection.…”

“…The aminolipid-deficient mutant is less susceptible to phage attachment We have previously shown that PlcP-mediated membrane lipid remodelling imposes trade-offs for the survival of Phaeobacter sp. MED193 [29]. To further understand the ecological importance of these aminolipids, we compared the ability of phage DSS3-Phi2, the first known bacteriophage to infect Ruegeria pomeroyi DSS-3 [26], to bind to the WT and the olsA mutant.…”

Competition–defense trade-offs in the microbial world

“…In PNAS, Guillonneau et al. ( 1 ) report experiments that demonstrate a rather intricate trade-off in the predator–prey relationship between a bacterium and its protozoan predator. Trade-offs link positive to negative changes in fitness and therefore constrain the paths of evolution as well as the biodiversity, structure, and function of existing food webs.…”

“…Guillonneau et al.’s ( 1 ) study addresses a response strategy to phosphorus (P) limitation found in many prokaryotes: the substitution of phospholipids with sulfolipids ( 9 ), reducing their requirement for P. Since this only occurs under P limitation, the substitution seems to have a fitness cost, only worth paying when P is a scarce commodity. Both lipid groups are surface-active compounds, and the reduction in P requirement likely comes with the side effect of a change in cell surface properties.…”

“…The trade-off studied by Guillonneau et al. ( 1 ) is thus part of a highly connected system where trade-offs influence food web structure, food web structure influences ocean chemistry, and ocean chemistry influences trade-offs. Guillonneau et al.…”