The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571

Lee, Kyung-Bum; Backer, Philippe De; Aono, Toshihiro; Liu, Chi-Te; Suzuki, Shino; Suzuki, Tamiko; Kaneko, Takakazu; Yamada, Manabu; Tabata, Satoshi; Kupfer, Doris M.; Najar, Fares Z.; Wiley, Graham B.; Roe, Bruce A.; Binnewies, Tim T.; Ussery, David W.; D’Haeze, Wim; Herder, Jeroen Den; Gevers, Dirk; Vereecke, Danny; Holsters, Marcelle; Oyaizu, Hiroshi

doi:10.1186/1471-2164-9-271

Cited by 115 publications

(88 citation statements)

References 74 publications

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“…Rhizobial genomes are subdivided into genome regions specific for their life stages, with chromosomal loci expressed during free-living phases in the soil and symbiosis loci expressed inside of host cells [13,14]. Symbiosis loci required for host nodulation and nitrogen fixation are clustered onto large plasmids or genomic islands [15][16][17][18][19], that can be transferred among lineages, presumably via conjugation [20][21][22]. Non-nodulating rhizobia are also common [23,24], and these strains often lack some or all of the characterized symbiosis loci [23][24][25][26][27][28].…”

Section: Introductionmentioning

confidence: 99%

Epidemic Spread of Symbiotic and Non-Symbiotic Bradyrhizobium Genotypes Across California

et al. 2015

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The patterns and drivers of bacterial strain dominance remain poorly understood in natural populations. Here, we cultured 1292 Bradyrhizobium isolates from symbiotic root nodules and the soil root interface of the host plant Acmispon strigosus across a >840-km transect in California. To investigate epidemiology and the potential role of accessory loci as epidemic drivers, isolates were genotyped at two chromosomal loci and were assayed for presence or absence of accessory Bsymbiosis island^loci that encode capacity to form nodules on hosts. We found that Bradyrhizobium populations were very diverse but dominated by few haplotypeswith a single Bepidemic^haplotype constituting nearly 30 % of collected isolates and spreading nearly statewide. In many Bradyrhizobium lineages, we inferred presence and absence of the symbiosis island suggesting recurrent evolutionary gain and or loss of symbiotic capacity. We did not find statistical phylogenetic evidence that the symbiosis island acquisition promotes strain dominance and both symbiotic and nonsymbiotic strains exhibited population dominance and spatial spread. Our dataset reveals that a strikingly few Bradyrhizobium genotypes can rapidly spread to dominate a landscape and suggests that these epidemics are not driven by the acquisition of accessory loci as occurs in key human pathogens.

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Section: Introductionmentioning

confidence: 99%

Epidemic Spread of Symbiotic and Non-Symbiotic Bradyrhizobium Genotypes Across California

et al. 2015

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“…Analysis of the A. caulinodans ORS571 genome (10) revealed that its 87.6-kb symbiosis region, which contains three nodulation loci that are involved in the biosynthesis of Nod factors, has typical characteristics of a symbiosis island: It has a lower GC content and is inserted adjacent to a glytRNA gene. This region also contains genes related to conjugal transfer, transposases, and integrases ( Fig.…”

Section: A Caulinodans Symbiosis Island Ice Ac Can Horizontally Tranmentioning

confidence: 99%

Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island

Ling

Wang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Horizontal gene transfer (HGT) of genomic islands is a driving force of bacterial evolution. Many pathogens and symbionts use this mechanism to spread mobile genetic elements that carry genes important for interaction with their eukaryotic hosts. However, the role of the host in this process remains unclear. Here, we show that plant compounds inducing the nodulation process in the rhizobium-legume mutualistic symbiosis also enhance the transfer of symbiosis islands. We demonstrate that the symbiosis island of the Sesbania rostrata symbiont, Azorhizobium caulinodans, is an 87.6-kb integrative and conjugative element (ICE Ac ) that is able to excise, form a circular DNA, and conjugatively transfer to a specific site of gly-tRNA gene of other rhizobial genera, expanding their host range. The HGT frequency was significantly increased in the rhizosphere. An ICE Aclocated LysR-family transcriptional regulatory protein AhaR triggered the HGT process in response to plant flavonoids that induce the expression of nodulation genes through another LysR-type protein, NodD. Our study suggests that rhizobia may sense rhizosphere environments and transfer their symbiosis gene contents to other genera of rhizobia, thereby broadening rhizobial host-range specificity.horizontal gene transfer | host-range | integrative and conjugative element | naringenin | nodulation

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“…N 2 -fixing nodules are formed by A. caulinodans on the stems as well as on the roots of S. rostrata. Previously, the whole genome sequence of A. caulinodans was determined (Lee et al, 2008), and we performed a concurrent large-scale screening of rhizobial genetic factors involved in nodule development using A. caulinodans mutants created by random Tn5 mutagenesis (Suzuki et al, 2007). As a result of this screening, we isolated three mutants having a Tn5-insertion in the putative LPS biosynthesis genes (Suzuki et al, 2007).…”

Section: Effects Of Alteration In Lps Structure In Azorhizobium Caulimentioning

confidence: 99%

Effects of alteration in LPS structure in <i>Azorhizobium caulinodans</i> on nodule development

Wakao

Siarot

Aono

et al. 2015

J. Gen. Appl. Microbiol.

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2005). LPS is composed of three parts: lipid A, containing sugar and fatty acid, which forms the outer leaflet of the outer membrane and anchors LPS to the cell envelope; a core oligosaccharide region, a non-repeating oligosaccharide, which links lipid A and O-antigen; and the Oantigen, consisting of repeating oligosaccharide units. The LPS containing or lacking O-antigen is usually called smooth LPS and rough LPS, respectively. In the majority of gram-negative bacteria, the core oligosaccharide can be subdivided into an outer core and an inner core. The outer core region provides an attachment site for O-antigen. The inner core typically contains residues of 3-deoxy-D -manno-2-octulosonic acid (Kdo) and L-glycero-Dmanno-heptose. Kdo connects the inner core to the lipid A (Heinrichs et al., 1998;Raetz and Whitfield, 2002).Azorhizobium caulinodans ORS571 is a microsymbiont of a tropical legume, Sesbania rostrata (Dreyfus and Dommergues, 1981;Dreyfus et al., 1983Dreyfus et al., , 1988. N 2 -fixing nodules are formed by A. caulinodans on the stems as well as on the roots of S. rostrata. Previously, the whole genome sequence of A. caulinodans was determined (Lee et al., 2008), and we performed a concurrent large-scale screening of rhizobial genetic factors involved in nodule development using A. caulinodans mutants created by random Tn5 mutagenesis (Suzuki et al., 2007). As a result of this screening, we isolated three mutants having a Tn5-insertion in the putative LPS biosynthesis genes (Suzuki et al., 2007). These three mutants, Ao13-C11, Ao77-C09 and Ao80-F04, were disrupted in the rfaF, rfaD, and rfaE genes, respectively. These genes are involved in the synthesis of the LPS inner core region. The rfaD and rfaE genes encode ADP-L-glycero-D-manno-heptose-6-epimerase and ADP-L-glycero-D-manno-heptose synthase, respectively. These enzymes are involved in the synthesis of ADP-L-glycero-D-manno-heptose, which is a component of the LPS inner core (Kneidinger et al., 2002; The lipopolysaccharide (LPS) of Azorhizobium caulinodans ORS571, which forms N 2 -fixing nodules on the stems and roots of Sesbania rostrata, is known to be a positive signal required for the progression of nodule formation. In this study, four A. caulinodans mutants producing a variety of defective LPSs were compared. The LPSs of the mutants having Tn5 insertion in the rfaF, rfaD, and rfaE genes were more truncated than the modified LPSs of the oac2 mutants. However, the nodule formation by the rfaF, rfaD, and rfaE mutants was more advanced than that of the oac2 mutant, suggesting that invasion ability depends on the LPS structure. Our hypothesis is that not only the wild-type LPSs but also the altered LPSs of the oac2 mutant may be recognized as signal molecules by plants. The altered LPSs may act as negative signals that halt the symbiotic process, whereas the wild-type LPSs may prevent the halt of the symbiotic process. The more truncated LPSs of the rfaF, rfaD, and rfaE mutants perhaps no longer function as negative signals inducing discontinu...

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The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571

Cited by 115 publications

References 74 publications

Epidemic Spread of Symbiotic and Non-Symbiotic Bradyrhizobium Genotypes Across California

Epidemic Spread of Symbiotic and Non-Symbiotic Bradyrhizobium Genotypes Across California

Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island

Effects of alteration in LPS structure in <i>Azorhizobium caulinodans</i> on nodule development

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