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Associated bacteria affect sexual reproduction by altering gene expression and metabolic processes in a biofilm inhabiting diatom

Emilio Cirri, Sam De Decker, Gust Bilcke (UGent) , Markus Werner, Cristina Osuna, Lieven De Veylder (UGent) , Klaas Vandepoele (UGent) , Oliver Werz, Wim Vyverman (UGent) and Georg Pohnert
(2019) FRONTIERS IN MICROBIOLOGY. 10.
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Abstract
Diatoms are unicellular algae with a fundamental role in global biogeochemical cycles as major primary producers at the base of aquatic food webs. In recent years, chemical communication between diatoms and associated bacteria has emerged as a key factor in diatom ecology, spurred by conceptual and technological advancements to study the mechanisms underlying these interactions. Here, we use a combination of physiological, transcriptomic, and metabolomic approaches to study the influence of naturally coexisting bacteria, Maribacter sp. and Roseovarius sp., on the sexual reproduction of the biofilm inhabiting marine pennate diatom Seminavis robusta. While Maribacter sp. severely reduces the reproductive success of S. robusta cultures, Roseovarius sp. slightly enhances it. Contrary to our expectation, we demonstrate that the effect of the bacterial exudates is not caused by altered cell-cycle regulation prior to the switch to meiosis. Instead, Maribacter sp. exudates cause a reduced production of diproline, the sexual attraction pheromone of S. robusta. Transcriptomic analyses show that this is likely an indirect consequence of altered intracellular metabolic fluxes in the diatom, especially those related to amino acid biosynthesis, oxidative stress response, and biosynthesis of defense molecules. This study provides the first insights into the influence of bacteria on diatom sexual reproduction and adds a new dimension to the complexity of a still understudied phenomenon in natural diatom populations.
Keywords
pheromones, diatoms, bacterial exudates, cross-kingdom interactions, metabolomics, transcriptomics, GLUTATHIONE TRANSFERASES, MARINE-BACTERIA, FATTY-ACIDS, BIOSYNTHESIS, DEFENSE, GROWTH, LIGHT, PHYTOPLANKTON, ACCLIMATION, ANNOTATION

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MLA
Cirri, Emilio, et al. “Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom.” FRONTIERS IN MICROBIOLOGY, vol. 10, 2019, doi:10.3389/fmicb.2019.01790.
APA
Cirri, E., De Decker, S., Bilcke, G., Werner, M., Osuna, C., De Veylder, L., … Pohnert, G. (2019). Associated bacteria affect sexual reproduction by altering gene expression and metabolic processes in a biofilm inhabiting diatom. FRONTIERS IN MICROBIOLOGY, 10. https://doi.org/10.3389/fmicb.2019.01790
Chicago author-date
Cirri, Emilio, Sam De Decker, Gust Bilcke, Markus Werner, Cristina Osuna, Lieven De Veylder, Klaas Vandepoele, Oliver Werz, Wim Vyverman, and Georg Pohnert. 2019. “Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom.” FRONTIERS IN MICROBIOLOGY 10. https://doi.org/10.3389/fmicb.2019.01790.
Chicago author-date (all authors)
Cirri, Emilio, Sam De Decker, Gust Bilcke, Markus Werner, Cristina Osuna, Lieven De Veylder, Klaas Vandepoele, Oliver Werz, Wim Vyverman, and Georg Pohnert. 2019. “Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom.” FRONTIERS IN MICROBIOLOGY 10. doi:10.3389/fmicb.2019.01790.
Vancouver
1.
Cirri E, De Decker S, Bilcke G, Werner M, Osuna C, De Veylder L, et al. Associated bacteria affect sexual reproduction by altering gene expression and metabolic processes in a biofilm inhabiting diatom. FRONTIERS IN MICROBIOLOGY. 2019;10.
IEEE
[1]
E. Cirri et al., “Associated bacteria affect sexual reproduction by altering gene expression and metabolic processes in a biofilm inhabiting diatom,” FRONTIERS IN MICROBIOLOGY, vol. 10, 2019.
@article{8624324,
  abstract     = {{Diatoms are unicellular algae with a fundamental role in global biogeochemical cycles as major primary producers at the base of aquatic food webs. In recent years, chemical communication between diatoms and associated bacteria has emerged as a key factor in diatom ecology, spurred by conceptual and technological advancements to study the mechanisms underlying these interactions. Here, we use a combination of physiological, transcriptomic, and metabolomic approaches to study the influence of naturally coexisting bacteria, Maribacter sp. and Roseovarius sp., on the sexual reproduction of the biofilm inhabiting marine pennate diatom Seminavis robusta. While Maribacter sp. severely reduces the reproductive success of S. robusta cultures, Roseovarius sp. slightly enhances it. Contrary to our expectation, we demonstrate that the effect of the bacterial exudates is not caused by altered cell-cycle regulation prior to the switch to meiosis. Instead, Maribacter sp. exudates cause a reduced production of diproline, the sexual attraction pheromone of S. robusta. Transcriptomic analyses show that this is likely an indirect consequence of altered intracellular metabolic fluxes in the diatom, especially those related to amino acid biosynthesis, oxidative stress response, and biosynthesis of defense molecules. This study provides the first insights into the influence of bacteria on diatom sexual reproduction and adds a new dimension to the complexity of a still understudied phenomenon in natural diatom populations.}},
  articleno    = {{1790}},
  author       = {{Cirri, Emilio and De Decker, Sam and Bilcke, Gust and Werner, Markus and Osuna, Cristina and De Veylder, Lieven and Vandepoele, Klaas and Werz, Oliver and Vyverman, Wim and Pohnert, Georg}},
  issn         = {{1664-302X}},
  journal      = {{FRONTIERS IN MICROBIOLOGY}},
  keywords     = {{pheromones,diatoms,bacterial exudates,cross-kingdom interactions,metabolomics,transcriptomics,GLUTATHIONE TRANSFERASES,MARINE-BACTERIA,FATTY-ACIDS,BIOSYNTHESIS,DEFENSE,GROWTH,LIGHT,PHYTOPLANKTON,ACCLIMATION,ANNOTATION}},
  language     = {{eng}},
  pages        = {{20}},
  title        = {{Associated bacteria affect sexual reproduction by altering gene expression and metabolic processes in a biofilm inhabiting diatom}},
  url          = {{http://doi.org/10.3389/fmicb.2019.01790}},
  volume       = {{10}},
  year         = {{2019}},
}
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