The central role of selenium in the biochemistry and ecology of the harmful pelagophyte, Aureococcus anophagefferens

Gobler, CJ; Lobanov, AV; Tang, YZ; Turanov, AA; Zhang, Y; Doblin, M; Taylor, GT; Sañudo-Wilhelmy, SA; Grigoriev, IV; Gladyshev, VN

The central role of selenium in the biochemistry and ecology of the harmful pelagophyte, Aureococcus anophagefferens

Gobler, CJ Lobanov, AV Tang, YZ Turanov, AA Zhang, Y

Doblin, M

Taylor, GT Sañudo-Wilhelmy, SA Grigoriev, IV Gladyshev, VN

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Publication Type:: Journal Article
Citation:: ISME Journal, 2013, 7 (7), pp. 1333 - 1343
Issue Date:: 2013-07-01

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Field	Value	Language
dc.contributor.author	Gobler, CJ	en_US
dc.contributor.author	Lobanov, AV	en_US
dc.contributor.author	Tang, YZ	en_US
dc.contributor.author	Turanov, AA	en_US
dc.contributor.author	Zhang, Y https://orcid.org/0000-0001-6490-6133	en_US
dc.contributor.author	Doblin, M https://orcid.org/0000-0001-8750-3433	en_US
dc.contributor.author	Taylor, GT	en_US
dc.contributor.author	Sañudo-Wilhelmy, SA	en_US
dc.contributor.author	Grigoriev, IV	en_US
dc.contributor.author	Gladyshev, VN	en_US
dc.date.issued	2013-07-01	en_US
dc.identifier.citation	ISME Journal, 2013, 7 (7), pp. 1333 - 1343	en_US
dc.identifier.issn	1751-7362	en_US
dc.identifier.uri	http://hdl.handle.net/10453/26534
dc.description.abstract	The trace element selenium (Se) is required for the biosynthesis of selenocysteine (Sec), the 21st amino acid in the genetic code, but its role in the ecology of harmful algal blooms (HABs) is unknown. Here, we examined the role of Se in the biology and ecology of the harmful pelagophyte, Aureococcus anophagefferens, through cell culture, genomic analyses, and ecosystem studies. This organism has the largest and the most diverse selenoproteome identified to date that consists of at least 59 selenoproteins, including known eukaryotic selenoproteins, selenoproteins previously only detected in bacteria, and novel selenoproteins. The A. anophagefferens selenoproteome was dominated by the thioredoxin fold proteins and oxidoreductase functions were assigned to the majority of detected selenoproteins. Insertion of Sec in these proteins was supported by a unique Sec insertion sequence. Se was required for the growth of A. anophagefferens as cultures grew maximally at nanomolar Se concentrations. In a coastal ecosystem, dissolved Se concentrations were elevated before and after A. anophagefferens blooms, but were reduced by >95% during the peak of blooms to 0.05 nM. Consistent with this pattern, enrichment of seawater with selenite before and after a bloom did not affect the growth of A. anophagefferens, but enrichment during the peak of the bloom significantly increased population growth rates. These findings demonstrate that Se inventories, which can be anthropogenically enriched, can support proliferation of HABs, such as A. anophagefferens through its synthesis of a large arsenal of Se-dependent oxidoreductases that fine-tune cellular redox homeostasis. © 2013 International Society for Microbial Ecology All rights reserved.	en_US
dc.relation.ispartof	ISME Journal	en_US
dc.relation.isbasedon	10.1038/ismej.2013.25	en_US
dc.subject.classification	Microbiology	en_US
dc.subject.mesh	Chlamydomonas reinhardtii	en_US
dc.subject.mesh	Selenium	en_US
dc.subject.mesh	Trace Elements	en_US
dc.subject.mesh	Proteome	en_US
dc.subject.mesh	DNA Transposable Elements	en_US
dc.subject.mesh	Biochemistry	en_US
dc.subject.mesh	Ecology	en_US
dc.subject.mesh	Seawater	en_US
dc.subject.mesh	Genes, Protozoan	en_US
dc.subject.mesh	Selenoproteins	en_US
dc.subject.mesh	Stramenopiles	en_US
dc.title	The central role of selenium in the biochemistry and ecology of the harmful pelagophyte, Aureococcus anophagefferens	en_US
dc.type	Journal Article
utslib.citation.volume	7	en_US
utslib.for	0602 Ecology	en_US
utslib.for	05 Environmental Sciences	en_US
utslib.for	06 Biological Sciences	en_US
utslib.for	10 Technology	en_US
pubs.embargo.period	Not known	en_US
pubs.organisational-group	/University of Technology Sydney
pubs.organisational-group	/University of Technology Sydney/Faculty of Health
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Strength - C3 - Climate Change Cluster
utslib.copyright.status	closed_access
pubs.issue	7	en_US
pubs.publication-status	Published	en_US
pubs.volume	7	en_US

Abstract:

The trace element selenium (Se) is required for the biosynthesis of selenocysteine (Sec), the 21st amino acid in the genetic code, but its role in the ecology of harmful algal blooms (HABs) is unknown. Here, we examined the role of Se in the biology and ecology of the harmful pelagophyte, Aureococcus anophagefferens, through cell culture, genomic analyses, and ecosystem studies. This organism has the largest and the most diverse selenoproteome identified to date that consists of at least 59 selenoproteins, including known eukaryotic selenoproteins, selenoproteins previously only detected in bacteria, and novel selenoproteins. The A. anophagefferens selenoproteome was dominated by the thioredoxin fold proteins and oxidoreductase functions were assigned to the majority of detected selenoproteins. Insertion of Sec in these proteins was supported by a unique Sec insertion sequence. Se was required for the growth of A. anophagefferens as cultures grew maximally at nanomolar Se concentrations. In a coastal ecosystem, dissolved Se concentrations were elevated before and after A. anophagefferens blooms, but were reduced by >95% during the peak of blooms to 0.05 nM. Consistent with this pattern, enrichment of seawater with selenite before and after a bloom did not affect the growth of A. anophagefferens, but enrichment during the peak of the bloom significantly increased population growth rates. These findings demonstrate that Se inventories, which can be anthropogenically enriched, can support proliferation of HABs, such as A. anophagefferens through its synthesis of a large arsenal of Se-dependent oxidoreductases that fine-tune cellular redox homeostasis. © 2013 International Society for Microbial Ecology All rights reserved.

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http://hdl.handle.net/10453/26534