Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin

S. Borin; L. Brusetti; F. Mapelli; G. D'Auria; T. Brusa; M. Marzorati; A. Rizzi; M. Yakimov; D. Marty; G.J. de Lange; P. Van der Wielen; H. Bolhuis; T.J. McGenity; P.N. Polymenakou; E. Malinverno; L. Giuliano; C. Corselli; D. Daffonchio

doi:10.1073/pnas.0811984106

Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin

S. Borin, L. Brusetti, F. Mapelli, G. D'Auria, T. Brusa, M. Marzorati, A. Rizzi, M. Yakimov, D. Marty, G.J. de Lange, P. Van der Wielen, H. Bolhuis, T.J. McGenity, P.N. Polymenakou, E. Malinverno, L. Giuliano, C. Corselli, D. Daffonchio

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Abstract

Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulfide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurem! ents, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines delta- and epsilon-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis.

Original language	English
Pages (from-to)	9151-9156
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	106
Issue number	23
DOIs	https://doi.org/10.1073/pnas.0811984106
Publication status	Published - 2009

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Borin, S., Brusetti, L., Mapelli, F., D'Auria, G., Brusa, T., Marzorati, M., Rizzi, A., Yakimov, M., Marty, D., de Lange, G. J., Van der Wielen, P., Bolhuis, H., McGenity, T. J., Polymenakou, P. N., Malinverno, E., Giuliano, L., Corselli, C., & Daffonchio, D. (2009). Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin. Proceedings of the National Academy of Sciences of the United States of America, 106(23), 9151-9156. https://doi.org/10.1073/pnas.0811984106

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title = "Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin",

abstract = "Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulfide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurem! ents, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines delta- and epsilon-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis.",

author = "S. Borin and L. Brusetti and F. Mapelli and G. D'Auria and T. Brusa and M. Marzorati and A. Rizzi and M. Yakimov and D. Marty and {de Lange}, G.J. and {Van der Wielen}, P. and H. Bolhuis and T.J. McGenity and P.N. Polymenakou and E. Malinverno and L. Giuliano and C. Corselli and D. Daffonchio",

note = "Reporting year: 2009 Metis note: 4571;CEME; MM; file:///L:/Endnotedatabases/NIOOPUB/pdfs/PDFS2009\Borin_ea_4571.pdf",

year = "2009",

doi = "10.1073/pnas.0811984106",

language = "English",

volume = "106",

pages = "9151--9156",

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Borin, S, Brusetti, L, Mapelli, F, D'Auria, G, Brusa, T, Marzorati, M, Rizzi, A, Yakimov, M, Marty, D, de Lange, GJ, Van der Wielen, P, Bolhuis, H, McGenity, TJ, Polymenakou, PN, Malinverno, E, Giuliano, L, Corselli, C & Daffonchio, D 2009, 'Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin', Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 23, pp. 9151-9156. https://doi.org/10.1073/pnas.0811984106

Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin. / Borin, S.; Brusetti, L.; Mapelli, F. et al.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 23, 2009, p. 9151-9156.

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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T1 - Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin

AU - Borin, S.

AU - Brusetti, L.

AU - Mapelli, F.

AU - D'Auria, G.

AU - Brusa, T.

AU - Marzorati, M.

AU - Rizzi, A.

AU - Yakimov, M.

AU - Marty, D.

AU - de Lange, G.J.

AU - Van der Wielen, P.

AU - Bolhuis, H.

AU - McGenity, T.J.

AU - Polymenakou, P.N.

AU - Malinverno, E.

AU - Giuliano, L.

AU - Corselli, C.

AU - Daffonchio, D.

N1 - Reporting year: 2009 Metis note: 4571;CEME; MM; file:///L:/Endnotedatabases/NIOOPUB/pdfs/PDFS2009\Borin_ea_4571.pdf

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N2 - Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulfide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurem! ents, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines delta- and epsilon-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis.

AB - Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulfide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurem! ents, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines delta- and epsilon-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis.

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DO - 10.1073/pnas.0811984106

M3 - Article

SN - 0027-8424

VL - 106

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 23

ER -

Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin

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