Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria
Abstract Background Jellyfish blooms represent a significant but largely overlooked source of labile organic matter (jelly-OM) in the ocean, characterized by a high protein content. Decaying jellyfish are important carriers for carbon export to the ocean’s interior. To accurately incorporate them in...
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| Format: | Article |
| Language: | English |
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BMC
2023-07-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01598-8 |
| _version_ | 1797774030340620288 |
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| author | Tinkara Tinta Zihao Zhao Barbara Bayer Gerhard J. Herndl |
| author_facet | Tinkara Tinta Zihao Zhao Barbara Bayer Gerhard J. Herndl |
| author_sort | Tinkara Tinta |
| collection | DOAJ |
| description | Abstract Background Jellyfish blooms represent a significant but largely overlooked source of labile organic matter (jelly-OM) in the ocean, characterized by a high protein content. Decaying jellyfish are important carriers for carbon export to the ocean’s interior. To accurately incorporate them into biogeochemical models, the interactions between microbes and jelly-OM have yet to be fully characterized. We conducted jelly-OM enrichment experiments in microcosms to simulate the scenario experienced by the coastal pelagic microbiome after the decay of a jellyfish bloom. We combined metagenomics, endo- and exo-metaproteomic approaches to obtain a mechanistic understanding on the metabolic network operated by the jelly-OM degrading bacterial consortium. Results Our analysis revealed that OM released during the decay of jellyfish blooms triggers a rapid shuffling of the taxonomic and functional profile of the pelagic bacterial community, resulting in a significant enrichment of protein/amino acid catabolism-related enzymes in the jelly-OM degrading community dominated by Pseudoalteromonadaceae, Alteromonadaceae and Vibrionaceae, compared to unamended control treatments. In accordance with the proteinaceous character of jelly-OM, Pseudoalteromonadaceae synthesized and excreted enzymes associated with proteolysis, while Alteromonadaceae contributed to extracellular hydrolysis of complex carbohydrates and organophosphorus compounds. In contrast, Vibrionaceae synthesized transporter proteins for peptides, amino acids and carbohydrates, exhibiting a cheater-type lifestyle, i.e. benefiting from public goods released by others. In the late stage of jelly-OM degradation, Rhodobacteraceae and Alteromonadaceae became dominant, growing on jelly-OM left-overs or bacterial debris, potentially contributing to the accumulation of dissolved organic nitrogen compounds and inorganic nutrients, following the decay of jellyfish blooms. Conclusions Our findings indicate that specific chemical and metabolic fingerprints associated with decaying jellyfish blooms are substantially different to those previously associated with decaying phytoplankton blooms, potentially altering the functioning and biogeochemistry of marine systems. We show that decaying jellyfish blooms are associated with the enrichment in extracellular collagenolytic bacterial proteases, which could act as virulence factors in human and marine organisms’ disease, with possible implications for marine ecosystem services. Our study also provides novel insights into niche partitioning and metabolic interactions among key jelly-OM degraders operating a complex metabolic network in a temporal cascade of biochemical reactions to degrade pulses of jellyfish-bloom-specific compounds in the water column. Video Abstract |
| first_indexed | 2024-03-12T22:15:01Z |
| format | Article |
| id | doaj.art-81c923d2b537428d9321c9059b48b5c1 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-12T22:15:01Z |
| publishDate | 2023-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-81c923d2b537428d9321c9059b48b5c12023-07-23T11:20:34ZengBMCMicrobiome2049-26182023-07-0111112210.1186/s40168-023-01598-8Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteriaTinkara Tinta0Zihao Zhao1Barbara Bayer2Gerhard J. Herndl3Marine Biology Station Piran, National Institute of BiologyDepartment of Functional and Evolutionary Ecology, Bio-Oceanography and Marine Biology Unit, University of ViennaDepartment of Microbiology and Ecosystem Science, Centre for Microbiology and Environmental Systems Science, University of ViennaDepartment of Functional and Evolutionary Ecology, Bio-Oceanography and Marine Biology Unit, University of ViennaAbstract Background Jellyfish blooms represent a significant but largely overlooked source of labile organic matter (jelly-OM) in the ocean, characterized by a high protein content. Decaying jellyfish are important carriers for carbon export to the ocean’s interior. To accurately incorporate them into biogeochemical models, the interactions between microbes and jelly-OM have yet to be fully characterized. We conducted jelly-OM enrichment experiments in microcosms to simulate the scenario experienced by the coastal pelagic microbiome after the decay of a jellyfish bloom. We combined metagenomics, endo- and exo-metaproteomic approaches to obtain a mechanistic understanding on the metabolic network operated by the jelly-OM degrading bacterial consortium. Results Our analysis revealed that OM released during the decay of jellyfish blooms triggers a rapid shuffling of the taxonomic and functional profile of the pelagic bacterial community, resulting in a significant enrichment of protein/amino acid catabolism-related enzymes in the jelly-OM degrading community dominated by Pseudoalteromonadaceae, Alteromonadaceae and Vibrionaceae, compared to unamended control treatments. In accordance with the proteinaceous character of jelly-OM, Pseudoalteromonadaceae synthesized and excreted enzymes associated with proteolysis, while Alteromonadaceae contributed to extracellular hydrolysis of complex carbohydrates and organophosphorus compounds. In contrast, Vibrionaceae synthesized transporter proteins for peptides, amino acids and carbohydrates, exhibiting a cheater-type lifestyle, i.e. benefiting from public goods released by others. In the late stage of jelly-OM degradation, Rhodobacteraceae and Alteromonadaceae became dominant, growing on jelly-OM left-overs or bacterial debris, potentially contributing to the accumulation of dissolved organic nitrogen compounds and inorganic nutrients, following the decay of jellyfish blooms. Conclusions Our findings indicate that specific chemical and metabolic fingerprints associated with decaying jellyfish blooms are substantially different to those previously associated with decaying phytoplankton blooms, potentially altering the functioning and biogeochemistry of marine systems. We show that decaying jellyfish blooms are associated with the enrichment in extracellular collagenolytic bacterial proteases, which could act as virulence factors in human and marine organisms’ disease, with possible implications for marine ecosystem services. Our study also provides novel insights into niche partitioning and metabolic interactions among key jelly-OM degraders operating a complex metabolic network in a temporal cascade of biochemical reactions to degrade pulses of jellyfish-bloom-specific compounds in the water column. Video Abstracthttps://doi.org/10.1186/s40168-023-01598-8Jellyfish detritusMicrobial consortiaMetagenomicsMetaproteomicsExoproteomics |
| spellingShingle | Tinkara Tinta Zihao Zhao Barbara Bayer Gerhard J. Herndl Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria Microbiome Jellyfish detritus Microbial consortia Metagenomics Metaproteomics Exoproteomics |
| title | Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria |
| title_full | Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria |
| title_fullStr | Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria |
| title_full_unstemmed | Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria |
| title_short | Jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria |
| title_sort | jellyfish detritus supports niche partitioning and metabolic interactions among pelagic marine bacteria |
| topic | Jellyfish detritus Microbial consortia Metagenomics Metaproteomics Exoproteomics |
| url | https://doi.org/10.1186/s40168-023-01598-8 |
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