Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya
Abstract 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 organi...
Main Authors: | , , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2019-02-01
|
Series: | Microbiome |
Subjects: | |
Online Access: | http://link.springer.com/article/10.1186/s40168-019-0643-4 |
_version_ | 1818837104380084224 |
---|---|
author | So-Jeong Kim Jong-Geol Kim Sang-Hoon Lee Soo-Je Park Joo-Han Gwak Man-Young Jung Won-Hyung Chung Eun-Jin Yang Jisoo Park Jinyoung Jung Yoonsoo Hahn Jang-Cheon Cho Eugene L. Madsen Francisco Rodriguez-Valera Jung-Ho Hyun Sung-Keun Rhee |
author_facet | So-Jeong Kim Jong-Geol Kim Sang-Hoon Lee Soo-Je Park Joo-Han Gwak Man-Young Jung Won-Hyung Chung Eun-Jin Yang Jisoo Park Jinyoung Jung Yoonsoo Hahn Jang-Cheon Cho Eugene L. Madsen Francisco Rodriguez-Valera Jung-Ho Hyun Sung-Keun Rhee |
author_sort | So-Jeong Kim |
collection | DOAJ |
description | Abstract 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. |
first_indexed | 2024-12-19T03:17:12Z |
format | Article |
id | doaj.art-ba5a30758f744765b7b1cc54967fe445 |
institution | Directory Open Access Journal |
issn | 2049-2618 |
language | English |
last_indexed | 2024-12-19T03:17:12Z |
publishDate | 2019-02-01 |
publisher | BMC |
record_format | Article |
series | Microbiome |
spelling | doaj.art-ba5a30758f744765b7b1cc54967fe4452022-12-21T20:37:51ZengBMCMicrobiome2049-26182019-02-017111510.1186/s40168-019-0643-4Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynyaSo-Jeong Kim0Jong-Geol Kim1Sang-Hoon Lee2Soo-Je Park3Joo-Han Gwak4Man-Young Jung5Won-Hyung Chung6Eun-Jin Yang7Jisoo Park8Jinyoung Jung9Yoonsoo Hahn10Jang-Cheon Cho11Eugene L. Madsen12Francisco Rodriguez-Valera13Jung-Ho Hyun14Sung-Keun Rhee15Geologic Environment Research Division, Korea Institute of Geoscience and Mineral ResourcesDepartment of Microbiology, Chungbuk National UniversityDivision of Polar Ocean Environment, Korea Polar Research InstituteDepartment of Biology, Jeju National UniversityDepartment of Microbiology, Chungbuk National UniversityDepartment of Microbial Ecology, University of ViennaResearch Group of Gut Microbiome, Korea Food Research InstituteDivision of Polar Ocean Environment, Korea Polar Research InstituteDivision of Polar Ocean Environment, Korea Polar Research InstituteDivision of Polar Ocean Environment, Korea Polar Research InstituteDepartment of Life Science, Chung-Ang UniversityDepartment of Biological Sciences, Inha UniversityDepartment of Microbiology, Cornell UniversityEvolutionary Genomics Group, División de Microbiología, Universidad Miguel HernándezDepartment of Marine Science and Convergence Engineering, Hanyang University ERICA CampusDepartment of Microbiology, Chungbuk National UniversityAbstract 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.http://link.springer.com/article/10.1186/s40168-019-0643-4Carbon remineralizationGenomicsMetatranscriptomicsPolynya |
spellingShingle | So-Jeong Kim Jong-Geol Kim Sang-Hoon Lee Soo-Je Park Joo-Han Gwak Man-Young Jung Won-Hyung Chung Eun-Jin Yang Jisoo Park Jinyoung Jung Yoonsoo Hahn Jang-Cheon Cho Eugene L. Madsen Francisco Rodriguez-Valera Jung-Ho Hyun Sung-Keun Rhee Genomic and metatranscriptomic analyses of carbon remineralization in an Antarctic polynya Microbiome Carbon remineralization Genomics Metatranscriptomics 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 | Carbon remineralization Genomics Metatranscriptomics Polynya |
url | http://link.springer.com/article/10.1186/s40168-019-0643-4 |
work_keys_str_mv | AT sojeongkim genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT jonggeolkim genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT sanghoonlee genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT soojepark genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT joohangwak genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT manyoungjung genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT wonhyungchung genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT eunjinyang genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT jisoopark genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT jinyoungjung genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT yoonsoohahn genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT jangcheoncho genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT eugenelmadsen genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT franciscorodriguezvalera genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT junghohyun genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya AT sungkeunrhee genomicandmetatranscriptomicanalysesofcarbonremineralizationinanantarcticpolynya |