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Bacterial lifestyle switch in response to algal metabolites

View ORCID ProfileNoa Barak-Gavish, View ORCID ProfileBareket Dassa, View ORCID ProfileConstanze Kuhlisch, Inbal Nussbaum, Gili Rosenberg, View ORCID ProfileRoi Avraham, View ORCID ProfileAssaf Vardi
doi: https://doi.org/10.1101/2022.01.10.475657
Noa Barak-Gavish
1Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel
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Bareket Dassa
2Bioinformatics Unit, Department of Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot 7610001, Israel
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Constanze Kuhlisch
1Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel
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Inbal Nussbaum
1Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel
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Gili Rosenberg
3Department of Biological Regulation, Weizmann Institute of Science, Rehovot 7610001, Israel
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Roi Avraham
3Department of Biological Regulation, Weizmann Institute of Science, Rehovot 7610001, Israel
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Assaf Vardi
1Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot 7610001, Israel
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  • For correspondence: assaf.vardi@weizmann.ac.il
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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 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 profiled bacterial transcriptomes in response to infochemicals derived from algae in exponential and stationary growth, which induced the Sulfitobacter D7 coexistence and pathogenicity lifestyles, respectively. We found that algal dimethylsulfoniopropionate (DMSP) was a pivotal signaling molecule that mediated the transition between the lifestyles. However, the coexisting and pathogenic lifestyles were evident only in the presence of additional algal metabolites. In the pathogenic mode, Sulfitobacter D7 upregulated flagellar motility and many transport systems, presumably to maximize assimilation of E. huxleyi-derived metabolites released by algal cells upon cell death. Specifically, we discovered that algae-produced benzoate promoted the growth of Sulfitobacter D7, and negated the DMSP-inducing 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 status of the algal host through changes in the metabolic composition, which will determine the bacterial lifestyle during the interactions.

Significance Statement Microorganisms in the marine environment play crucial roles in the regulation of Earth’s climate and elemental cycling. Understanding microbial interactions and the metabolic exchange that drives them is necessary for disentangling the complexity of the marine ecosystem. Here we demonstrate how the opportunistic pathogen Sulfitobacter D7 switches its lifestyle from coexistence to pathogenicity in response to metabolites released by Emiliania huxleyi, a bloom-forming unicellular alga. By mapping bacterial transcriptional profiles, we show that the algal metabolite dimethylsulfoniopropionate (DMSP), an important signaling molecule in the marine environment, is essential for the bacterial lifestyle switch. However, the activity of DMSP depended on additional algal signals. This work emphasizes how metabolic crosstalk can influence the nature and fate of microbial interactions, which have cascading effects on large-scale oceanic processes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Competing Interest Statement: The authors declare that they have no competing interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 10, 2022.
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Bacterial lifestyle switch in response to algal metabolites
Noa Barak-Gavish, Bareket Dassa, Constanze Kuhlisch, Inbal Nussbaum, Gili Rosenberg, Roi Avraham, Assaf Vardi
bioRxiv 2022.01.10.475657; doi: https://doi.org/10.1101/2022.01.10.475657
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Bacterial lifestyle switch in response to algal metabolites
Noa Barak-Gavish, Bareket Dassa, Constanze Kuhlisch, Inbal Nussbaum, Gili Rosenberg, Roi Avraham, Assaf Vardi
bioRxiv 2022.01.10.475657; doi: https://doi.org/10.1101/2022.01.10.475657

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