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Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers

Helen Decleyre (UGent) , Kim Heylen (UGent) , Bjorn Tytgat (UGent) and Anne Willems (UGent)
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Organization
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BOF-UGent GOA 01G01911
Abstract
Background: Copper dependent nitrite reductase, NirK, catalyses the key step in denitrification, i.e. nitrite reduction to nitric oxide. Distinct structural NirK classes and phylogenetic clades of NirK-type denitrifiers have previously been observed based on a limited set of NirK sequences, however, their environmental distribution or ecological strategies are currently unknown. In addition, environmental nirK-type denitrifiers are currently underestimated in PCR-dependent surveys due to primer coverage limitations that can be attributed to their broad taxonomic diversity and enormous nirK sequence divergence. Therefore, we revisited reported analyses on partial NirK sequences using a taxonomically diverse, full-length NirK sequence dataset. Results: Division of NirK sequences into two phylogenetically distinct clades was confirmed, with Clade I mainly comprising Alphaproteobacteria (plus some Gamma- and Betaproteobacteria) and Clade II harbouring more diverse taxonomic groups like Archaea, Bacteroidetes, Chloroflexi, Gemmatimonadetes, Nitrospirae, Firmicutes, Actinobacteria, Planctomycetes and Proteobacteria (mainly Beta and Gamma). Failure of currently available primer sets to target diverse NirK-type denitrifiers in environmental surveys could be attributed to mismatches over the whole length of the primer binding regions including the 3' site, with Clade II sequences containing higher sequence divergence than Clade I sequences. Simultaneous presence of both the denitrification and DNRA pathway could be observed in 67 % of all NirK-type denitrifiers. Conclusion: The previously reported division of NirK into two distinct phylogenetic clades was confirmed using a taxonomically diverse set of full-length NirK sequences. Enormous sequence divergence of nirK gene sequences, probably due to variable nirK evolutionary trajectories, will remain an issue for covering diverse NirK-type denitrifiers in amplicon-based environmental surveys. The potential of a single organism to partition nitrate to either denitrification or dissimilatory nitrate reduction to ammonium appeared to be more widespread than originally anticipated as more than half of all NirK-type denitrifiers were shown to contain both pathways in their genome.
Keywords
Sequence diversity, Genomic linkage, CuNIR, Classes of NirK, cNirK, CONTAINING NITRITE REDUCTASE, LOIHICA STRAIN PV-4, ESCHERICHIA-COLI, NITROUS-OXIDE, HYPHOMICROBIUM-DENITRIFICANS, CULTIVATED DENITRIFIERS, COMMUNITY COMPOSITION, NITRATE REDUCTASE, ELECTRON-TRANSFER, SIGNAL PEPTIDES

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Citation

Please use this url to cite or link to this publication:

MLA
Decleyre, Helen et al. “Highly Diverse nirK Genes Comprise Two Major Clades That Harbour Ammonium-producing Denitrifiers.” BMC GENOMICS 17 (2016): n. pag. Print.
APA
Decleyre, H., Heylen, K., Tytgat, B., & Willems, A. (2016). Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers. BMC GENOMICS, 17.
Chicago author-date
Decleyre, Helen, Kim Heylen, Bjorn Tytgat, and Anne Willems. 2016. “Highly Diverse nirK Genes Comprise Two Major Clades That Harbour Ammonium-producing Denitrifiers.” Bmc Genomics 17.
Chicago author-date (all authors)
Decleyre, Helen, Kim Heylen, Bjorn Tytgat, and Anne Willems. 2016. “Highly Diverse nirK Genes Comprise Two Major Clades That Harbour Ammonium-producing Denitrifiers.” Bmc Genomics 17.
Vancouver
1.
Decleyre H, Heylen K, Tytgat B, Willems A. Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers. BMC GENOMICS. 2016;17.
IEEE
[1]
H. Decleyre, K. Heylen, B. Tytgat, and A. Willems, “Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers,” BMC GENOMICS, vol. 17, 2016.
@article{7225429,
  abstract     = {Background: Copper dependent nitrite reductase, NirK, catalyses the key step in denitrification, i.e. nitrite reduction to nitric oxide. Distinct structural NirK classes and phylogenetic clades of NirK-type denitrifiers have previously been observed based on a limited set of NirK sequences, however, their environmental distribution or ecological strategies are currently unknown. In addition, environmental nirK-type denitrifiers are currently underestimated in PCR-dependent surveys due to primer coverage limitations that can be attributed to their broad taxonomic diversity and enormous nirK sequence divergence. Therefore, we revisited reported analyses on partial NirK sequences using a taxonomically diverse, full-length NirK sequence dataset. 
Results: Division of NirK sequences into two phylogenetically distinct clades was confirmed, with Clade I mainly comprising Alphaproteobacteria (plus some Gamma- and Betaproteobacteria) and Clade II harbouring more diverse taxonomic groups like Archaea, Bacteroidetes, Chloroflexi, Gemmatimonadetes, Nitrospirae, Firmicutes, Actinobacteria, Planctomycetes and Proteobacteria (mainly Beta and Gamma). Failure of currently available primer sets to target diverse NirK-type denitrifiers in environmental surveys could be attributed to mismatches over the whole length of the primer binding regions including the 3' site, with Clade II sequences containing higher sequence divergence than Clade I sequences. Simultaneous presence of both the denitrification and DNRA pathway could be observed in 67 % of all NirK-type denitrifiers. 
Conclusion: The previously reported division of NirK into two distinct phylogenetic clades was confirmed using a taxonomically diverse set of full-length NirK sequences. Enormous sequence divergence of nirK gene sequences, probably due to variable nirK evolutionary trajectories, will remain an issue for covering diverse NirK-type denitrifiers in amplicon-based environmental surveys. The potential of a single organism to partition nitrate to either denitrification or dissimilatory nitrate reduction to ammonium appeared to be more widespread than originally anticipated as more than half of all NirK-type denitrifiers were shown to contain both pathways in their genome.},
  articleno    = {155},
  author       = {Decleyre, Helen and Heylen, Kim and Tytgat, Bjorn and Willems, Anne},
  issn         = {1471-2164},
  journal      = {BMC GENOMICS},
  keywords     = {Sequence diversity,Genomic linkage,CuNIR,Classes of NirK,cNirK,CONTAINING NITRITE REDUCTASE,LOIHICA STRAIN PV-4,ESCHERICHIA-COLI,NITROUS-OXIDE,HYPHOMICROBIUM-DENITRIFICANS,CULTIVATED DENITRIFIERS,COMMUNITY COMPOSITION,NITRATE REDUCTASE,ELECTRON-TRANSFER,SIGNAL PEPTIDES},
  language     = {eng},
  pages        = {13},
  title        = {Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers},
  url          = {http://dx.doi.org/10.1186/s12864-016-2465-0},
  volume       = {17},
  year         = {2016},
}

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