Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean
Abstract Background Heterotrophic microbes in the Southern Ocean are challenged by the double constraint of low concentrations of organic carbon (C) and iron (Fe). These essential elements are tightly coupled in cellular processes; however, the prokaryotic requirements of C and Fe under varying envi...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-08-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01600-3 |
| _version_ | 1797452126008377344 |
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| author | Pavla Debeljak Barbara Bayer Ying Sun Gerhard J. Herndl Ingrid Obernosterer |
| author_facet | Pavla Debeljak Barbara Bayer Ying Sun Gerhard J. Herndl Ingrid Obernosterer |
| author_sort | Pavla Debeljak |
| collection | DOAJ |
| description | Abstract Background Heterotrophic microbes in the Southern Ocean are challenged by the double constraint of low concentrations of organic carbon (C) and iron (Fe). These essential elements are tightly coupled in cellular processes; however, the prokaryotic requirements of C and Fe under varying environmental settings remain poorly studied. Here, we used a combination of metatranscriptomics and metaproteomics to identify prokaryotic membrane transporters for organic substrates and Fe in naturally iron-fertilized and high-nutrient, low-chlorophyll waters of the Southern Ocean during spring and late summer. Results Pronounced differences in membrane transporter profiles between seasons were observed at both sites, both at the transcript and protein level. When specific compound classes were considered, the two approaches revealed different patterns. At the transcript level, seasonal patterns were only observed for subsets of genes belonging to each transporter category. At the protein level, membrane transporters of organic compounds were relatively more abundant in spring as compared to summer, while the opposite pattern was observed for Fe transporters. These observations suggest an enhanced requirement for organic C in early spring and for Fe in late summer. Mapping transcripts and proteins to 50 metagenomic-assembled genomes revealed distinct taxon-specific seasonal differences pointing to potentially opportunistic clades, such as Pseudomonadales and Nitrincolaceae, and groups with a more restricted repertoire of expressed transporters, such as Alphaproteobacteria and Flavobacteriaceae. Conclusion The combined investigations of C and Fe membrane transporters suggest seasonal changes in the microbial requirements of these elements under different productivity regimes. The taxon-specific acquisition strategies of different forms of C and Fe illustrate how diverse microbes could shape transcript and protein expression profiles at the community level at different seasons. Our results on the C- and Fe-related metabolic capabilities of microbial taxa provide new insights into their potential role in the cycling of C and Fe under varying nutrient regimes in the Southern Ocean. Video Abstract |
| first_indexed | 2024-03-09T15:03:17Z |
| format | Article |
| id | doaj.art-b7dfe6cb1dba4f07af239d0b4e978476 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-09T15:03:17Z |
| publishDate | 2023-08-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-b7dfe6cb1dba4f07af239d0b4e9784762023-11-26T13:47:37ZengBMCMicrobiome2049-26182023-08-0111111210.1186/s40168-023-01600-3Seasonal patterns in microbial carbon and iron transporter expression in the Southern OceanPavla Debeljak0Barbara Bayer1Ying Sun2Gerhard J. Herndl3Ingrid Obernosterer4Laboratoire d’Océanographie Microbienne (LOMIC), CNRS, Sorbonne UniversitéDepartment of Functional and Evolutionary Ecology, University of ViennaLaboratoire d’Océanographie Microbienne (LOMIC), CNRS, Sorbonne UniversitéDepartment of Functional and Evolutionary Ecology, University of ViennaLaboratoire d’Océanographie Microbienne (LOMIC), CNRS, Sorbonne UniversitéAbstract Background Heterotrophic microbes in the Southern Ocean are challenged by the double constraint of low concentrations of organic carbon (C) and iron (Fe). These essential elements are tightly coupled in cellular processes; however, the prokaryotic requirements of C and Fe under varying environmental settings remain poorly studied. Here, we used a combination of metatranscriptomics and metaproteomics to identify prokaryotic membrane transporters for organic substrates and Fe in naturally iron-fertilized and high-nutrient, low-chlorophyll waters of the Southern Ocean during spring and late summer. Results Pronounced differences in membrane transporter profiles between seasons were observed at both sites, both at the transcript and protein level. When specific compound classes were considered, the two approaches revealed different patterns. At the transcript level, seasonal patterns were only observed for subsets of genes belonging to each transporter category. At the protein level, membrane transporters of organic compounds were relatively more abundant in spring as compared to summer, while the opposite pattern was observed for Fe transporters. These observations suggest an enhanced requirement for organic C in early spring and for Fe in late summer. Mapping transcripts and proteins to 50 metagenomic-assembled genomes revealed distinct taxon-specific seasonal differences pointing to potentially opportunistic clades, such as Pseudomonadales and Nitrincolaceae, and groups with a more restricted repertoire of expressed transporters, such as Alphaproteobacteria and Flavobacteriaceae. Conclusion The combined investigations of C and Fe membrane transporters suggest seasonal changes in the microbial requirements of these elements under different productivity regimes. The taxon-specific acquisition strategies of different forms of C and Fe illustrate how diverse microbes could shape transcript and protein expression profiles at the community level at different seasons. Our results on the C- and Fe-related metabolic capabilities of microbial taxa provide new insights into their potential role in the cycling of C and Fe under varying nutrient regimes in the Southern Ocean. Video Abstracthttps://doi.org/10.1186/s40168-023-01600-3Prokaryotic membrane transportersOrganic substrate utilizationIron uptakeMetatranscriptomicsMetaproteomicsMetagenome-assembled genomes |
| spellingShingle | Pavla Debeljak Barbara Bayer Ying Sun Gerhard J. Herndl Ingrid Obernosterer Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean Microbiome Prokaryotic membrane transporters Organic substrate utilization Iron uptake Metatranscriptomics Metaproteomics Metagenome-assembled genomes |
| title | Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean |
| title_full | Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean |
| title_fullStr | Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean |
| title_full_unstemmed | Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean |
| title_short | Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean |
| title_sort | seasonal patterns in microbial carbon and iron transporter expression in the southern ocean |
| topic | Prokaryotic membrane transporters Organic substrate utilization Iron uptake Metatranscriptomics Metaproteomics Metagenome-assembled genomes |
| url | https://doi.org/10.1186/s40168-023-01600-3 |
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