Global contribution of pelagic fungi to protein degradation in the ocean
Abstract Background Fungi are important degraders of organic matter responsible for reintegration of nutrients into global food chains in freshwater and soil environments. Recent evidence suggests that they are ubiquitously present in the oceanic water column where they play an active role in the de...
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| Format: | Article |
| Language: | English |
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BMC
2022-09-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01329-5 |
| _version_ | 1811297508856430592 |
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| author | Eva Breyer Zihao Zhao Gerhard J. Herndl Federico Baltar |
| author_facet | Eva Breyer Zihao Zhao Gerhard J. Herndl Federico Baltar |
| author_sort | Eva Breyer |
| collection | DOAJ |
| description | Abstract Background Fungi are important degraders of organic matter responsible for reintegration of nutrients into global food chains in freshwater and soil environments. Recent evidence suggests that they are ubiquitously present in the oceanic water column where they play an active role in the degradation of carbohydrates. However, their role in processing other abundant biomolecules in the ocean in comparison with that of prokaryotes remains enigmatic. Here, we performed a global-ocean multi-omics analysis of all fungal-affiliated peptidases (main enzymes responsible for cleaving proteins), which constitute the major fraction (> 50%) of marine living and detrital biomass. We determined the abundance, expression, diversity, taxonomic affiliation, and functional classification of the genes encoding all pelagic fungal peptidases from the epi- and mesopelagic layers. Results We found that pelagic fungi are active contributors to protein degradation and nitrogen cycling in the global ocean. Dothideomycetes are the main fungi responsible for protease activity in the surface layers, whereas Leotiomycetes dominate in the mesopelagic realm. Gene abundance, diversity, and expression increased with increasing depth, similar to fungal CAZymes. This contrasts with the total occurrence of prokaryotic peptidases and CAZymes which are more uniformly distributed in the oceanic water column, suggesting potentially different ecological niches of fungi and prokaryotes. In-depth analysis of the most widely expressed fungal protease revealed the potentially dominating role of saprotrophic nutrition in the oceans. Conclusions Our findings expand the current knowledge on the role of oceanic fungi in the carbon cycle (carbohydrates) to the so far unknown global participation in nitrogen (proteins) degradation, highlighting potentially different ecological niches occupied by fungi and prokaryotes in the global ocean. Video Abstract |
| first_indexed | 2024-04-13T06:05:26Z |
| format | Article |
| id | doaj.art-ab0ab6b956c34a39b916f1e04995af26 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-13T06:05:26Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-ab0ab6b956c34a39b916f1e04995af262022-12-22T02:59:16ZengBMCMicrobiome2049-26182022-09-0110111110.1186/s40168-022-01329-5Global contribution of pelagic fungi to protein degradation in the oceanEva Breyer0Zihao Zhao1Gerhard J. Herndl2Federico Baltar3Department of Functional and Evolutionary Ecology, University of ViennaDepartment of Functional and Evolutionary Ecology, University of ViennaDepartment of Functional and Evolutionary Ecology, University of ViennaDepartment of Functional and Evolutionary Ecology, University of ViennaAbstract Background Fungi are important degraders of organic matter responsible for reintegration of nutrients into global food chains in freshwater and soil environments. Recent evidence suggests that they are ubiquitously present in the oceanic water column where they play an active role in the degradation of carbohydrates. However, their role in processing other abundant biomolecules in the ocean in comparison with that of prokaryotes remains enigmatic. Here, we performed a global-ocean multi-omics analysis of all fungal-affiliated peptidases (main enzymes responsible for cleaving proteins), which constitute the major fraction (> 50%) of marine living and detrital biomass. We determined the abundance, expression, diversity, taxonomic affiliation, and functional classification of the genes encoding all pelagic fungal peptidases from the epi- and mesopelagic layers. Results We found that pelagic fungi are active contributors to protein degradation and nitrogen cycling in the global ocean. Dothideomycetes are the main fungi responsible for protease activity in the surface layers, whereas Leotiomycetes dominate in the mesopelagic realm. Gene abundance, diversity, and expression increased with increasing depth, similar to fungal CAZymes. This contrasts with the total occurrence of prokaryotic peptidases and CAZymes which are more uniformly distributed in the oceanic water column, suggesting potentially different ecological niches of fungi and prokaryotes. In-depth analysis of the most widely expressed fungal protease revealed the potentially dominating role of saprotrophic nutrition in the oceans. Conclusions Our findings expand the current knowledge on the role of oceanic fungi in the carbon cycle (carbohydrates) to the so far unknown global participation in nitrogen (proteins) degradation, highlighting potentially different ecological niches occupied by fungi and prokaryotes in the global ocean. Video Abstracthttps://doi.org/10.1186/s40168-022-01329-5Pelagic fungiProteasesMetagenomicsMetatranscriptomicsGlobal oceanNitrogen cycle |
| spellingShingle | Eva Breyer Zihao Zhao Gerhard J. Herndl Federico Baltar Global contribution of pelagic fungi to protein degradation in the ocean Microbiome Pelagic fungi Proteases Metagenomics Metatranscriptomics Global ocean Nitrogen cycle |
| title | Global contribution of pelagic fungi to protein degradation in the ocean |
| title_full | Global contribution of pelagic fungi to protein degradation in the ocean |
| title_fullStr | Global contribution of pelagic fungi to protein degradation in the ocean |
| title_full_unstemmed | Global contribution of pelagic fungi to protein degradation in the ocean |
| title_short | Global contribution of pelagic fungi to protein degradation in the ocean |
| title_sort | global contribution of pelagic fungi to protein degradation in the ocean |
| topic | Pelagic fungi Proteases Metagenomics Metatranscriptomics Global ocean Nitrogen cycle |
| url | https://doi.org/10.1186/s40168-022-01329-5 |
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