Symbiotic burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical High-Affinity cytochrome cbb3 Oxidase genes

Sofie E. De Meyer, Leah Briscoe, Pilar Martínez-Hidalgo, Christina M. Agapakis, Paulina Estrada De-Los Santos, Rekha Seshadri, Wayne Reeve, George Weinstock, Graham O'Hara, John G. Howieson, Ann M. Hirsch

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Genome analysis of fourteen mimosoid and four papilionoid beta-rhizobia together with fourteen reference alpha-rhizobia for both nodulation (nod) and nitrogen-fixing (nif/fix) genes has shown phylogenetic congruence between 16S rRNA/MLSA (combined 16S rRNA gene sequencing and multilocus sequence analysis) and nif/fix genes, indicating a free-living diazotrophic ancestry of the beta-rhizobia. However, deeper genomic analysis revealed a complex symbiosis acquisition history in the betarhizobia that clearly separates the mimosoid and papilionoid nodulating groups. Mimosoid-nodulating beta-rhizobia have nod genes tightly clustered in the nodBCIJHASU operon, whereas papilionoid-nodulating Burkholderia have nodUSDABC and nodIJ genes, although their arrangement is not canonical because the nod genes are subdivided by the insertion of nif and other genes. Furthermore, the papilionoid Burkholderia spp. contain duplications of several nod and nif genes. The Burkholderia nifHDKEN and fixABC genes are very closely related to those found in free-living diazotrophs. In contrast, nifA is highly divergent between both groups, but the papilionoid species nifA is more similar to alpha-rhizobia nifA than to other groups. Surprisingly, for all Burkholderia, the fixNOQP and fixGHIS genes required for cbb3 cytochrome oxidase production and assembly are missing. In contrast, symbiotic Cupriavidus strains have fixNOQPGHIS genes, revealing a divergence in the evolution of two distinct electron transport chains required for nitrogen fixation within the beta-rhizobia.

Original languageEnglish
Pages (from-to)609-619
Number of pages11
JournalMolecular Plant-Microbe Interactions
Volume29
Issue number8
DOIs
StatePublished - 1 Jan 2016

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Burkholderia
nodulation
cytochrome-c oxidase
Rhizobium
Genes
genes
Cupriavidus
cbb3 oxidase
Multilocus Sequence Typing
Nitrogen Fixation
ribosomal RNA
Symbiosis
Insertional Mutagenesis
Operon
Electron Transport
nitrogen-fixing bacteria
rRNA Genes
electron transport chain
operon
Nitrogen

Cite this

De Meyer, Sofie E. ; Briscoe, Leah ; Martínez-Hidalgo, Pilar ; Agapakis, Christina M. ; De-Los Santos, Paulina Estrada ; Seshadri, Rekha ; Reeve, Wayne ; Weinstock, George ; O'Hara, Graham ; Howieson, John G. ; Hirsch, Ann M. / Symbiotic burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical High-Affinity cytochrome cbb3 Oxidase genes. In: Molecular Plant-Microbe Interactions. 2016 ; Vol. 29, No. 8. pp. 609-619.
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abstract = "Genome analysis of fourteen mimosoid and four papilionoid beta-rhizobia together with fourteen reference alpha-rhizobia for both nodulation (nod) and nitrogen-fixing (nif/fix) genes has shown phylogenetic congruence between 16S rRNA/MLSA (combined 16S rRNA gene sequencing and multilocus sequence analysis) and nif/fix genes, indicating a free-living diazotrophic ancestry of the beta-rhizobia. However, deeper genomic analysis revealed a complex symbiosis acquisition history in the betarhizobia that clearly separates the mimosoid and papilionoid nodulating groups. Mimosoid-nodulating beta-rhizobia have nod genes tightly clustered in the nodBCIJHASU operon, whereas papilionoid-nodulating Burkholderia have nodUSDABC and nodIJ genes, although their arrangement is not canonical because the nod genes are subdivided by the insertion of nif and other genes. Furthermore, the papilionoid Burkholderia spp. contain duplications of several nod and nif genes. The Burkholderia nifHDKEN and fixABC genes are very closely related to those found in free-living diazotrophs. In contrast, nifA is highly divergent between both groups, but the papilionoid species nifA is more similar to alpha-rhizobia nifA than to other groups. Surprisingly, for all Burkholderia, the fixNOQP and fixGHIS genes required for cbb3 cytochrome oxidase production and assembly are missing. In contrast, symbiotic Cupriavidus strains have fixNOQPGHIS genes, revealing a divergence in the evolution of two distinct electron transport chains required for nitrogen fixation within the beta-rhizobia.",
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De Meyer, SE, Briscoe, L, Martínez-Hidalgo, P, Agapakis, CM, De-Los Santos, PE, Seshadri, R, Reeve, W, Weinstock, G, O'Hara, G, Howieson, JG & Hirsch, AM 2016, 'Symbiotic burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical High-Affinity cytochrome cbb3 Oxidase genes', Molecular Plant-Microbe Interactions, vol. 29, no. 8, pp. 609-619. https://doi.org/10.1094/MPMI-05-16-0091-R

Symbiotic burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical High-Affinity cytochrome cbb3 Oxidase genes. / De Meyer, Sofie E.; Briscoe, Leah; Martínez-Hidalgo, Pilar; Agapakis, Christina M.; De-Los Santos, Paulina Estrada; Seshadri, Rekha; Reeve, Wayne; Weinstock, George; O'Hara, Graham; Howieson, John G.; Hirsch, Ann M.

In: Molecular Plant-Microbe Interactions, Vol. 29, No. 8, 01.01.2016, p. 609-619.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Symbiotic burkholderia species show diverse arrangements of nif/fix and nod genes and lack typical High-Affinity cytochrome cbb3 Oxidase genes

AU - De Meyer, Sofie E.

AU - Briscoe, Leah

AU - Martínez-Hidalgo, Pilar

AU - Agapakis, Christina M.

AU - De-Los Santos, Paulina Estrada

AU - Seshadri, Rekha

AU - Reeve, Wayne

AU - Weinstock, George

AU - O'Hara, Graham

AU - Howieson, John G.

AU - Hirsch, Ann M.

PY - 2016/1/1

Y1 - 2016/1/1

N2 - Genome analysis of fourteen mimosoid and four papilionoid beta-rhizobia together with fourteen reference alpha-rhizobia for both nodulation (nod) and nitrogen-fixing (nif/fix) genes has shown phylogenetic congruence between 16S rRNA/MLSA (combined 16S rRNA gene sequencing and multilocus sequence analysis) and nif/fix genes, indicating a free-living diazotrophic ancestry of the beta-rhizobia. However, deeper genomic analysis revealed a complex symbiosis acquisition history in the betarhizobia that clearly separates the mimosoid and papilionoid nodulating groups. Mimosoid-nodulating beta-rhizobia have nod genes tightly clustered in the nodBCIJHASU operon, whereas papilionoid-nodulating Burkholderia have nodUSDABC and nodIJ genes, although their arrangement is not canonical because the nod genes are subdivided by the insertion of nif and other genes. Furthermore, the papilionoid Burkholderia spp. contain duplications of several nod and nif genes. The Burkholderia nifHDKEN and fixABC genes are very closely related to those found in free-living diazotrophs. In contrast, nifA is highly divergent between both groups, but the papilionoid species nifA is more similar to alpha-rhizobia nifA than to other groups. Surprisingly, for all Burkholderia, the fixNOQP and fixGHIS genes required for cbb3 cytochrome oxidase production and assembly are missing. In contrast, symbiotic Cupriavidus strains have fixNOQPGHIS genes, revealing a divergence in the evolution of two distinct electron transport chains required for nitrogen fixation within the beta-rhizobia.

AB - Genome analysis of fourteen mimosoid and four papilionoid beta-rhizobia together with fourteen reference alpha-rhizobia for both nodulation (nod) and nitrogen-fixing (nif/fix) genes has shown phylogenetic congruence between 16S rRNA/MLSA (combined 16S rRNA gene sequencing and multilocus sequence analysis) and nif/fix genes, indicating a free-living diazotrophic ancestry of the beta-rhizobia. However, deeper genomic analysis revealed a complex symbiosis acquisition history in the betarhizobia that clearly separates the mimosoid and papilionoid nodulating groups. Mimosoid-nodulating beta-rhizobia have nod genes tightly clustered in the nodBCIJHASU operon, whereas papilionoid-nodulating Burkholderia have nodUSDABC and nodIJ genes, although their arrangement is not canonical because the nod genes are subdivided by the insertion of nif and other genes. Furthermore, the papilionoid Burkholderia spp. contain duplications of several nod and nif genes. The Burkholderia nifHDKEN and fixABC genes are very closely related to those found in free-living diazotrophs. In contrast, nifA is highly divergent between both groups, but the papilionoid species nifA is more similar to alpha-rhizobia nifA than to other groups. Surprisingly, for all Burkholderia, the fixNOQP and fixGHIS genes required for cbb3 cytochrome oxidase production and assembly are missing. In contrast, symbiotic Cupriavidus strains have fixNOQPGHIS genes, revealing a divergence in the evolution of two distinct electron transport chains required for nitrogen fixation within the beta-rhizobia.

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U2 - 10.1094/MPMI-05-16-0091-R

DO - 10.1094/MPMI-05-16-0091-R

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AN - SCOPUS:84989849150

VL - 29

SP - 609

EP - 619

JO - Molecular Plant-Microbe Interactions

JF - Molecular Plant-Microbe Interactions

SN - 0894-0282

IS - 8

ER -