Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae
IntroductionSeagrass meadows serve as an integral component of coastal ecosystems but are declining rapidly due to numerous anthropogenic stressors including climate change. Eelgrass wasting disease, caused by opportunistic Labyrinthula spp., is an increasing concern with rising seawater temperature...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2023.1152647/full |
| _version_ | 1797751826296078336 |
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| author | Yaamini R. Venkataraman Amanda Shore Sukanya Dayal James Sanghyun Lee Mahsa Alidoost Salimi Grace Crandall Malina M. Loeher Mark Stoops Megan Swanger Morgan E. Eisenlord Kathryn L. Van Alstyne Mark D. Fast Colleen A. Burge Colleen A. Burge Maya L. Groner Maya L. Groner |
| author_facet | Yaamini R. Venkataraman Amanda Shore Sukanya Dayal James Sanghyun Lee Mahsa Alidoost Salimi Grace Crandall Malina M. Loeher Mark Stoops Megan Swanger Morgan E. Eisenlord Kathryn L. Van Alstyne Mark D. Fast Colleen A. Burge Colleen A. Burge Maya L. Groner Maya L. Groner |
| author_sort | Yaamini R. Venkataraman |
| collection | DOAJ |
| description | IntroductionSeagrass meadows serve as an integral component of coastal ecosystems but are declining rapidly due to numerous anthropogenic stressors including climate change. Eelgrass wasting disease, caused by opportunistic Labyrinthula spp., is an increasing concern with rising seawater temperature. To better understand the host-pathogen interaction, we paired whole organism physiological assays with dual transcriptomic analysis of the infected host and parasite. MethodsEelgrass (Zostera marina) shoots were placed in one of two temperature treatments, 11° C or 18° C, acclimated for 10 days, and exposed to a waterborne inoculation containing infectious Labyrinthula zosterae (Lz) or sterile seawater. At two- and five-days post-exposure, pathogen load, visible disease signs, whole leaf phenolic content, and both host- and pathogen- transcriptomes were characterized. ResultsTwo days after exposure, more than 90% of plants had visible lesions and Lz DNA was detectable in 100% percent of sampled plants in the Lz exposed treatment. Concentrations of total phenolic compounds were lower after 5 days of combined exposure to warmer temperatures and Lz, but were unaffected in other treatments. Concentrations of condensed tannins were not affected by Lz or temperature, and did not change over time. Analysis of the eelgrass transcriptome revealed 540 differentially expressed genes in response to Lz exposure, but not temperature. Lz-exposed plants had gene expression patterns consistent with increased defense responses through altered regulation of phytohormone biosynthesis, stress response, and immune function pathways. Analysis of the pathogen transcriptome revealed up-regulation of genes potentially involved in breakdown of host defense, chemotaxis, phagocytosis, and metabolism. DiscussionThe lack of a significant temperature signal was unexpected but suggests a more pronounced physiological response to Lz infection as compared to temperature. Pre-acclimation of eelgrass plants to the temperature treatments may have contributed to the limited physiological responses to temperature. Collectively, these data characterize a widespread physiological response to pathogen attack and demonstrate the value of paired transcriptomics to understand infections in a host-pathogen system. |
| first_indexed | 2024-03-12T16:54:14Z |
| format | Article |
| id | doaj.art-0431966bd5904ecb95fe29b7bb0f0175 |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-03-12T16:54:14Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-0431966bd5904ecb95fe29b7bb0f01752023-08-08T07:47:29ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452023-08-011010.3389/fmars.2023.11526471152647Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosteraeYaamini R. Venkataraman0Amanda Shore1Sukanya Dayal2James Sanghyun Lee3Mahsa Alidoost Salimi4Grace Crandall5Malina M. Loeher6Mark Stoops7Megan Swanger8Morgan E. Eisenlord9Kathryn L. Van Alstyne10Mark D. Fast11Colleen A. Burge12Colleen A. Burge13Maya L. Groner14Maya L. Groner15Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United StatesDepartment of Biology, Farmingdale State College, Farmingdale, NY, United StatesInstitute of Marine & Environmental Technology, University of Maryland Baltimore County, University of Maryland Baltimore, Baltimore, MD, United StatesSchool of Marine and Environmental Affairs, University of Washington, Seattle, WA, United StatesSchool of Geography, Earth and Atmospheric Sciences, University of Melbourne, Victoria, VIC, AustraliaSchool of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, United StatesDepartment of Aquatic Health Sciences, Virginia Institute of Marine Science, Gloucester Point, VA, United StatesUniversity of North Carolina (UNC) Chapel Hill Institute of Marine Sciences, Morehead City, NC, United StatesSchool of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, United StatesDepartment of Ecology and Evolutionary Biology, Cornell University Corson Hall, Ithaca, NY, United States0Shannon Point Marine Center, Western Washington University, Anacortes, WA, United States1Hoplite Lab, Department of Pathology and Microbiology, Atlantic Veterinary College-University of Prince Edward Island (AVC-UPEI), Charlottetown, PE, CanadaInstitute of Marine & Environmental Technology, University of Maryland Baltimore County, University of Maryland Baltimore, Baltimore, MD, United States2Department of Microbiology, University of Maryland Baltimore, Baltimore, MD, United States1Hoplite Lab, Department of Pathology and Microbiology, Atlantic Veterinary College-University of Prince Edward Island (AVC-UPEI), Charlottetown, PE, Canada3Bigelow Lab for Ocean Sciences, East Boothbay, ME, United StatesIntroductionSeagrass meadows serve as an integral component of coastal ecosystems but are declining rapidly due to numerous anthropogenic stressors including climate change. Eelgrass wasting disease, caused by opportunistic Labyrinthula spp., is an increasing concern with rising seawater temperature. To better understand the host-pathogen interaction, we paired whole organism physiological assays with dual transcriptomic analysis of the infected host and parasite. MethodsEelgrass (Zostera marina) shoots were placed in one of two temperature treatments, 11° C or 18° C, acclimated for 10 days, and exposed to a waterborne inoculation containing infectious Labyrinthula zosterae (Lz) or sterile seawater. At two- and five-days post-exposure, pathogen load, visible disease signs, whole leaf phenolic content, and both host- and pathogen- transcriptomes were characterized. ResultsTwo days after exposure, more than 90% of plants had visible lesions and Lz DNA was detectable in 100% percent of sampled plants in the Lz exposed treatment. Concentrations of total phenolic compounds were lower after 5 days of combined exposure to warmer temperatures and Lz, but were unaffected in other treatments. Concentrations of condensed tannins were not affected by Lz or temperature, and did not change over time. Analysis of the eelgrass transcriptome revealed 540 differentially expressed genes in response to Lz exposure, but not temperature. Lz-exposed plants had gene expression patterns consistent with increased defense responses through altered regulation of phytohormone biosynthesis, stress response, and immune function pathways. Analysis of the pathogen transcriptome revealed up-regulation of genes potentially involved in breakdown of host defense, chemotaxis, phagocytosis, and metabolism. DiscussionThe lack of a significant temperature signal was unexpected but suggests a more pronounced physiological response to Lz infection as compared to temperature. Pre-acclimation of eelgrass plants to the temperature treatments may have contributed to the limited physiological responses to temperature. Collectively, these data characterize a widespread physiological response to pathogen attack and demonstrate the value of paired transcriptomics to understand infections in a host-pathogen system.https://www.frontiersin.org/articles/10.3389/fmars.2023.1152647/fullZostera marinaLabyrinthula zosteraeeelgrass wasting diseasetranscriptomicshost-pathogen interactionsmarine disease |
| spellingShingle | Yaamini R. Venkataraman Amanda Shore Sukanya Dayal James Sanghyun Lee Mahsa Alidoost Salimi Grace Crandall Malina M. Loeher Mark Stoops Megan Swanger Morgan E. Eisenlord Kathryn L. Van Alstyne Mark D. Fast Colleen A. Burge Colleen A. Burge Maya L. Groner Maya L. Groner Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae Frontiers in Marine Science Zostera marina Labyrinthula zosterae eelgrass wasting disease transcriptomics host-pathogen interactions marine disease |
| title | Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae |
| title_full | Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae |
| title_fullStr | Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae |
| title_full_unstemmed | Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae |
| title_short | Characterizing host-pathogen interactions between Zostera marina and Labyrinthula zosterae |
| title_sort | characterizing host pathogen interactions between zostera marina and labyrinthula zosterae |
| topic | Zostera marina Labyrinthula zosterae eelgrass wasting disease transcriptomics host-pathogen interactions marine disease |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2023.1152647/full |
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