Bacterial lifestyle switch in response to algal metabolites

Abstract

Unicellular algae, termed phytoplankton, greatly impact the marine environment by serving as the basis of marine food webs and by playing central roles in the biogeochemical cycling of elements. The interactions between phytoplankton and heterotrophic bacteria affect the fitness of both partners. It is becoming increasingly recognized that metabolic exchange determines the nature of such interactions, but the underlying molecular mechanisms remain underexplored. Here, we investigated the molecular and metabolic basis for the bacterial lifestyle switch, from coexistence to pathogenicity, in Sulfitobacter D7 during its interaction with Emiliania huxleyi, a cosmopolitan bloom-forming phytoplankter. To unravel the bacterial lifestyle switch, we analyzed bacterial transcriptomes in response to exudates derived from algae in exponential growth and stationary phase, which supported the Sulfitobacter D7 coexistence and pathogenicity lifestyles, respectively. In pathogenic mode, Sulfitobacter D7 upregulated flagellar motility and diverse transport systems, presumably to maximize assimilation of E. huxleyi-derived metabolites released by algal cells upon cell death. Algal dimethylsulfoniopropionate (DMSP) was a pivotal signaling molecule that mediated the transition between the lifestyles, supporting our previous findings. However, the coexisting and pathogenic lifestyles were evident only in the presence of additional algal metabolites. Specifically, we discovered that algae-produced benzoate promoted the growth of Sulfitobacter D7 and hindered the DMSP-induced lifestyle switch to pathogenicity, demonstrating that benzoate is important for maintaining the coexistence of algae and bacteria. We propose that bacteria can sense the physiological state of the algal host through changes in the metabolic composition, which will determine the bacterial lifestyle during interaction.

Cryptic bacterial pathogens of diatoms peak during senescence of a winter diatom bloom

“…This concept of a 'sliding scale' from synergistic to antagonistic is not new in marine microbial ecology. Jekyll-and-Hyde dynamics towards coccolithophores have also been observed for Rhodobacteraceae bacteria Phaeobacter (Seyedsayamdost et al, 2011) and Sulfitobacter (Barak-Gavish et al, 2018, 2023. However, our evidence suggests this 'switch' towards antagonistic behaviour may be more common than previously recognised, with the growth inhibitory effects of bacterial species spanning seven different bacterial orders tested being enhanced by pregrowth on DDM.…”

Cryptic bacterial pathogens of diatoms peak during senescence of a winter diatom bloom

“…However, we also observed differences in the dynamics of our system. Whereas Sulfitobacter D7 pregrown on ½YTSS 'coexisted' with the coccolithophore Emiliania huxleyi for c. 7 d before becoming pathogenic (Barak-Gavish et al, 2023), ½YTSS-grown P. alexandrii did not cause a culture crash of susceptible diatoms even after 16 d. In the E. huxleyi-Sulfitobacter system, the signalling molecule algal-derived dimethylsulfoniopropionate (DMSP) was identified to be pivotal for mediating the transition to pathogenicity, whereas benzoate hindered this switch (Barak-Gavish et al, 2023). Whether bacterial antagonists perceive different cues depending on the algal host remains an open question, particularly as diatoms are typically considered 'low DMSP producers' compared with coccolithophores (McParland & Levine, 2019).…”

“…This concept of a ‘sliding scale’ from synergistic to antagonistic is not new in marine microbial ecology. Jekyll‐and‐Hyde dynamics towards coccolithophores have also been observed for Rhodobacteraceae bacteria Phaeobacter (Seyedsayamdost et al ., 2011) and Sulfitobacter (Barak‐Gavish et al ., 2018, 2023). However, our evidence suggests this ‘switch’ towards antagonistic behaviour may be more common than previously recognised, with the growth inhibitory effects of bacterial species spanning seven different bacterial orders tested being enhanced by pregrowth on DDM.…”

Seed-to-Seed: Plant Core Vertically Transmitted Microbiota

“…Additionally, the relationship between plants and microbes may change when plants no longer require a particular microbe that has abandoned the genome. The extent to which this is the result of direct abandonment or gradual evolution, or whether the microbe can become pathogenic toward its host, remains an interesting question. , Further research is required to gain a better understanding of these questions and to deepen our knowledge of the coevolutionary relationship between plants and their vertically transmitted endophytes.…”