Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom
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...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-08-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.01790/full |
| _version_ | 1818204325558616064 |
|---|---|
| author | Emilio Cirri Sam De Decker Gust Bilcke Gust Bilcke Gust Bilcke Markus Werner Cristina Maria Osuna-Cruz Cristina Maria Osuna-Cruz Lieven De Veylder Lieven De Veylder Klaas Vandepoele Klaas Vandepoele Oliver Werz Wim Vyverman Georg Pohnert |
| author_facet | Emilio Cirri Sam De Decker Gust Bilcke Gust Bilcke Gust Bilcke Markus Werner Cristina Maria Osuna-Cruz Cristina Maria Osuna-Cruz Lieven De Veylder Lieven De Veylder Klaas Vandepoele Klaas Vandepoele Oliver Werz Wim Vyverman Georg Pohnert |
| author_sort | Emilio Cirri |
| collection | DOAJ |
| description | 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 co-existing 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. |
| first_indexed | 2024-12-12T03:39:27Z |
| format | Article |
| id | doaj.art-935ef883f1d64b81aef0151121a6a476 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-12T03:39:27Z |
| publishDate | 2019-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-935ef883f1d64b81aef0151121a6a4762022-12-22T00:39:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-08-011010.3389/fmicb.2019.01790469767Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting DiatomEmilio Cirri0Sam De Decker1Gust Bilcke2Gust Bilcke3Gust Bilcke4Markus Werner5Cristina Maria Osuna-Cruz6Cristina Maria Osuna-Cruz7Lieven De Veylder8Lieven De Veylder9Klaas Vandepoele10Klaas Vandepoele11Oliver Werz12Wim Vyverman13Georg Pohnert14Institute of Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, GermanyProtistology and Aquatic Ecology, Department of Biology, Ghent University, Ghent, BelgiumProtistology and Aquatic Ecology, Department of Biology, Ghent University, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Pharmaceutical/Medicinal Chemistry, Institute of Pharmacy, Friedrich-Schiller-University Jena, Jena, GermanyDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Pharmaceutical/Medicinal Chemistry, Institute of Pharmacy, Friedrich-Schiller-University Jena, Jena, GermanyProtistology and Aquatic Ecology, Department of Biology, Ghent University, Ghent, BelgiumInstitute of Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Jena, GermanyDiatoms 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 co-existing 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.01790/fullpheromonesdiatomsbacterial exudatescross-kingdom interactionsmetabolomicstranscriptomics |
| spellingShingle | Emilio Cirri Sam De Decker Gust Bilcke Gust Bilcke Gust Bilcke Markus Werner Cristina Maria Osuna-Cruz Cristina Maria Osuna-Cruz Lieven De Veylder Lieven De Veylder Klaas Vandepoele Klaas Vandepoele Oliver Werz Wim Vyverman Georg Pohnert Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom Frontiers in Microbiology pheromones diatoms bacterial exudates cross-kingdom interactions metabolomics transcriptomics |
| title | Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom |
| title_full | Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom |
| title_fullStr | Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom |
| title_full_unstemmed | Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom |
| title_short | Associated Bacteria Affect Sexual Reproduction by Altering Gene Expression and Metabolic Processes in a Biofilm Inhabiting Diatom |
| title_sort | associated bacteria affect sexual reproduction by altering gene expression and metabolic processes in a biofilm inhabiting diatom |
| topic | pheromones diatoms bacterial exudates cross-kingdom interactions metabolomics transcriptomics |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.01790/full |
| work_keys_str_mv | AT emiliocirri associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT samdedecker associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT gustbilcke associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT gustbilcke associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT gustbilcke associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT markuswerner associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT cristinamariaosunacruz associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT cristinamariaosunacruz associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT lievendeveylder associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT lievendeveylder associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT klaasvandepoele associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT klaasvandepoele associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT oliverwerz associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT wimvyverman associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom AT georgpohnert associatedbacteriaaffectsexualreproductionbyalteringgeneexpressionandmetabolicprocessesinabiofilminhabitingdiatom |