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Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya

BACKGROUND: Polynyas in the Southern Ocean are regions of intense primary production, mainly by Phaeocystis antarctica. Carbon fixed by phytoplankton in the water column is transferred to higher trophic levels, and finally, to the deep ocean. However, in the Amundsen Sea, most of this organic carbon...

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Autores principales: Kim, So-Jeong, Kim, Jong-Geol, Lee, Sang-Hoon, Park, Soo-Je, Gwak, Joo-Han, Jung, Man-Young, Chung, Won-Hyung, Yang, Eun-Jin, Park, Jisoo, Jung, Jinyoung, Hahn, Yoonsoo, Cho, Jang-Cheon, Madsen, Eugene L., Rodriguez-Valera, Francisco, Hyun, Jung-Ho, Rhee, Sung-Keun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6383258/
https://www.ncbi.nlm.nih.gov/pubmed/30786927
http://dx.doi.org/10.1186/s40168-019-0643-4
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author Kim, So-Jeong
Kim, Jong-Geol
Lee, Sang-Hoon
Park, Soo-Je
Gwak, Joo-Han
Jung, Man-Young
Chung, Won-Hyung
Yang, Eun-Jin
Park, Jisoo
Jung, Jinyoung
Hahn, Yoonsoo
Cho, Jang-Cheon
Madsen, Eugene L.
Rodriguez-Valera, Francisco
Hyun, Jung-Ho
Rhee, Sung-Keun
author_facet Kim, So-Jeong
Kim, Jong-Geol
Lee, Sang-Hoon
Park, Soo-Je
Gwak, Joo-Han
Jung, Man-Young
Chung, Won-Hyung
Yang, Eun-Jin
Park, Jisoo
Jung, Jinyoung
Hahn, Yoonsoo
Cho, Jang-Cheon
Madsen, Eugene L.
Rodriguez-Valera, Francisco
Hyun, Jung-Ho
Rhee, Sung-Keun
author_sort Kim, So-Jeong
collection PubMed
description BACKGROUND: Polynyas in the Southern Ocean are regions of intense primary production, mainly by Phaeocystis antarctica. Carbon fixed by phytoplankton in the water column is transferred to higher trophic levels, and finally, to the deep ocean. However, in the Amundsen Sea, most of this organic carbon does not reach the sediment but is degraded in the water column due to high bacterial heterotrophic activity. RESULTS: We reconstructed 12 key bacterial genomes from different phases of bloom and analyzed the expression of genes involved in organic carbon remineralization. A high correlation of gene expression between the peak and decline phases was observed in an individual genome bin-based pairwise comparison of gene expression. Polaribacter belonging to Bacteroidetes was found to be dominant in the peak phase, and its transcriptional activity was high (48.9% of the total mRNA reads). Two dominant Polaribacter bins had the potential to utilize major polymers in P. antarctica, chrysolaminarin and xylan, with a distinct set of glycosyl hydrolases. In the decline phase, Gammaproteobacteria (Ant4D3, SUP05, and SAR92), with the potential to utilize low molecular weight-dissolved organic matter (LMW-DOM) including compatible solutes, was increased. The versatility of Gammaproteobacteria may contribute to their abundance in organic carbon-rich polynya waters, while the SAR11 clade was found to be predominant in the sea ice-covered oligotrophic ocean. SAR92 clade showed transcriptional activity for utilization of both polysaccharides and LMW-DOM; this may account for their abundance both in the peak and decline phases. Ant4D3 clade was dominant in all phases of the polynya bloom, implicating the crucial roles of this clade in LMW-DOM remineralization in the Antarctic polynyas. CONCLUSIONS: Genomic reconstruction and in situ gene expression analyses revealed the unique metabolic potential of dominant bacteria of the Antarctic polynya at a finer taxonomic level. The information can be used to predict temporal community succession linked to the availability of substrates derived from the P. antarctica bloom. Global warming has resulted in compositional changes in phytoplankton from P. antarctica to diatoms, and thus, repeated parallel studies in various polynyas are required to predict global warming-related changes in carbon remineralization. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0643-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-63832582019-03-01 Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya Kim, So-Jeong Kim, Jong-Geol Lee, Sang-Hoon Park, Soo-Je Gwak, Joo-Han Jung, Man-Young Chung, Won-Hyung Yang, Eun-Jin Park, Jisoo Jung, Jinyoung Hahn, Yoonsoo Cho, Jang-Cheon Madsen, Eugene L. Rodriguez-Valera, Francisco Hyun, Jung-Ho Rhee, Sung-Keun Microbiome Research BACKGROUND: Polynyas in the Southern Ocean are regions of intense primary production, mainly by Phaeocystis antarctica. Carbon fixed by phytoplankton in the water column is transferred to higher trophic levels, and finally, to the deep ocean. However, in the Amundsen Sea, most of this organic carbon does not reach the sediment but is degraded in the water column due to high bacterial heterotrophic activity. RESULTS: We reconstructed 12 key bacterial genomes from different phases of bloom and analyzed the expression of genes involved in organic carbon remineralization. A high correlation of gene expression between the peak and decline phases was observed in an individual genome bin-based pairwise comparison of gene expression. Polaribacter belonging to Bacteroidetes was found to be dominant in the peak phase, and its transcriptional activity was high (48.9% of the total mRNA reads). Two dominant Polaribacter bins had the potential to utilize major polymers in P. antarctica, chrysolaminarin and xylan, with a distinct set of glycosyl hydrolases. In the decline phase, Gammaproteobacteria (Ant4D3, SUP05, and SAR92), with the potential to utilize low molecular weight-dissolved organic matter (LMW-DOM) including compatible solutes, was increased. The versatility of Gammaproteobacteria may contribute to their abundance in organic carbon-rich polynya waters, while the SAR11 clade was found to be predominant in the sea ice-covered oligotrophic ocean. SAR92 clade showed transcriptional activity for utilization of both polysaccharides and LMW-DOM; this may account for their abundance both in the peak and decline phases. Ant4D3 clade was dominant in all phases of the polynya bloom, implicating the crucial roles of this clade in LMW-DOM remineralization in the Antarctic polynyas. CONCLUSIONS: Genomic reconstruction and in situ gene expression analyses revealed the unique metabolic potential of dominant bacteria of the Antarctic polynya at a finer taxonomic level. The information can be used to predict temporal community succession linked to the availability of substrates derived from the P. antarctica bloom. Global warming has resulted in compositional changes in phytoplankton from P. antarctica to diatoms, and thus, repeated parallel studies in various polynyas are required to predict global warming-related changes in carbon remineralization. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0643-4) contains supplementary material, which is available to authorized users. BioMed Central 2019-02-20 /pmc/articles/PMC6383258/ /pubmed/30786927 http://dx.doi.org/10.1186/s40168-019-0643-4 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Kim, So-Jeong
Kim, Jong-Geol
Lee, Sang-Hoon
Park, Soo-Je
Gwak, Joo-Han
Jung, Man-Young
Chung, Won-Hyung
Yang, Eun-Jin
Park, Jisoo
Jung, Jinyoung
Hahn, Yoonsoo
Cho, Jang-Cheon
Madsen, Eugene L.
Rodriguez-Valera, Francisco
Hyun, Jung-Ho
Rhee, Sung-Keun
Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya
title Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya
title_full Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya
title_fullStr Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya
title_full_unstemmed Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya
title_short Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya
title_sort genomic and metatranscriptomic analyses of carbon remineralization in an antarctic polynya
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6383258/
https://www.ncbi.nlm.nih.gov/pubmed/30786927
http://dx.doi.org/10.1186/s40168-019-0643-4
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