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Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean
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 environmenta...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10439609/ https://www.ncbi.nlm.nih.gov/pubmed/37596690 http://dx.doi.org/10.1186/s40168-023-01600-3 |
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author | Debeljak, Pavla Bayer, Barbara Sun, Ying Herndl, Gerhard J. Obernosterer, Ingrid |
author_facet | Debeljak, Pavla Bayer, Barbara Sun, Ying Herndl, Gerhard J. Obernosterer, Ingrid |
author_sort | Debeljak, Pavla |
collection | PubMed |
description | 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01600-3. |
format | Online Article Text |
id | pubmed-10439609 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-104396092023-08-20 Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean Debeljak, Pavla Bayer, Barbara Sun, Ying Herndl, Gerhard J. Obernosterer, Ingrid Microbiome Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01600-3. BioMed Central 2023-08-19 /pmc/articles/PMC10439609/ /pubmed/37596690 http://dx.doi.org/10.1186/s40168-023-01600-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Debeljak, Pavla Bayer, Barbara Sun, Ying Herndl, Gerhard J. Obernosterer, Ingrid Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean |
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 | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10439609/ https://www.ncbi.nlm.nih.gov/pubmed/37596690 http://dx.doi.org/10.1186/s40168-023-01600-3 |
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