Complete Genome Sequence of the Model Rhizosphere Strain Azospirillum brasilense Az39, Successfully Applied in Agriculture

Rivera, Diego; Revale, Santiago; Molina, R.; Gualpa, José Luis; Puente, Mariana; Maroniche, Guillermo Andrés; París, Gastón; Baker, David; Clavijo, Bernardo; McLay, Kirsten; Spaepen, Stijn; Perticari, Alejandro; Vázquez, Martı́n; Wisniewski‐Dyé, Florence; Watkins, Christopher B.; Martı́nez-Abarca, Francisco; Vanderleyden, Jos; Cassán, Fabricio

doi:10.1128/genomea.00683-14

Cited by 39 publications

(27 citation statements)

References 18 publications

(16 reference statements)

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“…The DNA regions coding for CheA1 and for TMX are both located on the largest plasmid, p1, in all A. brasilense strains with available genome sequences, but they are not adjacent and are separated by several kilobases, precluding a simple frameshifting or slippage mutation between adjacent genes. Genome plasticity and extensive genomic rearrangements are evidenced in the Azospirillum genomes sequenced to date, including those of several strains of A. brasilense (34)(35)(36)(37)(38). These include the lack of synteny between replicons of strains from the same species, the abundance and density of insertion sequence IS elements in all genomes, and evidence of plasmid loss or rearrangements and of repeated phage infections.…”

Section: Discussionmentioning

confidence: 99%

“…None of the other Azospirillum species strains sequenced to date shows evidence of a similar domain insertion (34)(35)(36)(37)(38)(39). In fact, the draft genome of an Sp7 strain generated by a team of South Korean scientists also lacks the TMX fusion to CheA1 (NCBI BioProject PRJNA293508).…”

Section: Discussionmentioning

confidence: 99%

“…In fact, the draft genome of an Sp7 strain generated by a team of South Korean scientists also lacks the TMX fusion to CheA1 (NCBI BioProject PRJNA293508). A. brasilense genomes are organized as 7 replicons: one chromosome and 6 large plasmids named p1 through p6 (34)(35)(36)(37)(38)(39). The DNA regions coding for CheA1 and for TMX are both located on the largest plasmid, p1, in all A. brasilense strains with available genome sequences, but they are not adjacent and are separated by several kilobases, precluding a simple frameshifting or slippage mutation between adjacent genes.…”

Section: Discussionmentioning

confidence: 99%

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Distinct Domains of CheA Confer Unique Functions in Chemotaxis and Cell Length in Azospirillum brasilense Sp7

2017

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Chemotaxis is the movement of cells in response to gradients of diverse chemical cues. Motile bacteria utilize a conserved chemotaxis signal transduction system to bias their motility and navigate through a gradient. A central regulator of chemotaxis is the histidine kinase CheA. This cytoplasmic protein interacts with membrane-bound receptors, which assemble into large polar arrays, to propagate the signal. In the alphaproteobacterium Azospirillum brasilense, Che1 controls transient increases in swimming speed during chemotaxis, but it also biases the cell length at division. However, the exact underlying molecular mechanisms for Che1-dependent control of multiple cellular behaviors are not known. Here, we identify specific domains of the CheA1 histidine kinase implicated in modulating each of these functions. We show that CheA1 is produced in two isoforms: a membraneanchored isoform produced as a fusion with a conserved seven-transmembrane domain of unknown function (TMX) at the N terminus and a soluble isoform similar to prototypical CheA. Site-directed and deletion mutagenesis combined with behavioral assays confirm the role of CheA1 in chemotaxis and implicate the TMX domain in mediating changes in cell length. Fluorescence microscopy further reveals that the membrane-anchored isoform is distributed around the cell surface while the soluble isoform localizes at the cell poles. Together, the data provide a mechanism for the role of Che1 in controlling multiple unrelated cellular behaviors via acquisition of a new domain in CheA1 and production of distinct functional isoforms.IMPORTANCE Chemotaxis provides a significant competitive advantage to bacteria in the environment, and this function has been transferred laterally multiple times, with evidence of functional divergence in different genomic contexts. The molecular principles that underlie functional diversification of chemotaxis in various genomic contexts are unknown. Here, we provide a molecular mechanism by which a single CheA protein controls two unrelated functions: chemotaxis and cell length. Acquisition of this multifunctionality is seemingly a recent evolutionary event. The findings illustrate a mechanism by which chemotaxis function may be co-opted to regulate additional cellular functions.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Distinct Domains of CheA Confer Unique Functions in Chemotaxis and Cell Length in Azospirillum brasilense Sp7

2017

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“…In addition to regulating the probability of swimming reversals, motile A. brasilense cells navigating an attractant gradient can transiently increase their swimming speed (6). The available genome sequence of A. brasilense indicates the presence of four distinct chemotaxis operons, three (che1, che2, and che3) of which are also present in the genomes of all Azospirillum strains sequenced to date as well as in the genome of the closely related organism Rhodospirillum centenum (7)(8)(9)(10), suggesting that they were present in the last common ancestor of these two genera (Fig. 1).…”

mentioning

confidence: 99%

Azospirillum brasilense Chemotaxis Depends on Two Signaling Pathways Regulating Distinct Motility Parameters

et al. 2016

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The genomes of most motile bacteria encode two or more chemotaxis (Che) systems, but their functions have been characterized in only a few model systems. Azospirillum brasilense is a motile soil alphaproteobacterium able to colonize the rhizosphere of cereals. In response to an attractant, motile A. brasilense cells transiently increase swimming speed and suppress reversals. The Che1 chemotaxis pathway was previously shown to regulate changes in the swimming speed, but it has a minor role in chemotaxis and root surface colonization. Here, we show that a second chemotaxis system, named Che4, regulates the probability of swimming reversals and is the major signaling pathway for chemotaxis and wheat root surface colonization. Experimental evidence indicates that Che1 and Che4 are functionally linked to coordinate changes in the swimming motility pattern in response to attractants. The effect of Che1 on swimming speed is shown to enhance the aerotactic response of A. brasilense in gradients, likely providing the cells with a competitive advantage in the rhizosphere. Together, the results illustrate a novel mechanism by which motile bacteria utilize two chemotaxis pathways regulating distinct motility parameters to alter movement in gradients and enhance the chemotactic advantage. IMPORTANCEChemotaxis provides motile bacteria with a competitive advantage in the colonization of diverse niches and is a function enriched in rhizosphere bacterial communities, with most species possessing at least two chemotaxis systems. Here, we identify the mechanism by which cells may derive a significant chemotactic advantage using two chemotaxis pathways that ultimately regulate distinct motility parameters. Bacterial chemotaxis provides a competitive advantage by guiding motile cells in gradients of chemoeffectors toward environments that support growth and metabolism. Chemotaxis contributes to the establishment of various associations of bacteria with eukaryotic hosts (mammals, insects, and plants) and promotes virulence, symbiosis, and the establishment of microbial communities (1). Bacterial chemotaxis and motility are widespread traits encoded in the genomes of bacteria inhabiting diverse environments, and these functions are specifically enriched in microorganisms found in soils (2), suggesting that they provide a significant competitive advantage in this environment. Consistent with these findings, comparative genome analyses of chemotaxis in diverse motile bacteria suggested that most bacteria possess two chemotaxis systems and soil-dwelling bacteria often have more than two chemotaxis systems (3).The molecular mechanism of chemotaxis signal transduction has been deciphered in most detail in the model organism Escherichia coli, which possesses a single chemotaxis system. In E. coli, the chemotaxis signal transduction pathway consists of membrane-bound receptors clustered in dense arrays at the cell poles, where their C-terminal domains associate with cytoplasmic CheA kinase and the CheW scaffolding protein. When stimu...

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“…B510, A. amazonense Y2, and A. brasilense Sp245, CBG497, and Az39 (Kaneko et al 2010 ;Sant'Anna et al 2011 ;Wisniewski-Dyé et al 2011Rivera et al 2014 ). The complete genome sequences of the 3 A. brasilense strains and that of A. lipoferum 4B reveal no luxI homologue.…”

Section: Genome Analysesmentioning

confidence: 95%

Cell–Cell Communication in Azospirillum and Related PGPR

Wisniewski‐Dyé¹,

Vial²

2015

Handbook for Azospirillum

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Quorum-sensing (QS) regulation based on N -acyl-L -homoserine lactones (AHL) is used to control various phenotypes that are often essential for interaction with a eukaryotic host, notably for plant-associated bacteria. Technical methodologies currently used to reveal AHL production in a specifi c strain and to decipher phenotypes under QS regulation are surveyed in this chapter. Analyses conducted on the genus Azospirillum and on other related PGPR are used to illustrate the different steps of the approach. Among the genus Azospirillum , a survey of 40 strains belonging to six species revealed AHL production for four strains belonging to the lipoferum species or to a close undefi ned species and isolated from a rice rhizosphere. Identifi cation of genes mediating QS and regulating functions indicate that (1) distinct QS networks are present in some strains and seem to have been acquired independently by horizontal gene transfer; (2) QS regulation is strain specifi c with several phenotypes and numerous proteins being regulated by AHL-based QS in A. lipoferum B518, whereas no change is observed in A. lipoferum TVV3 defi cient in AHL production; and (3) QS is dedicated to regulating functions linked to rhizosphere competence and adaptation to plant roots in A. lipoferum B518.

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Complete Genome Sequence of the Model Rhizosphere Strain Azospirillum brasilense Az39, Successfully Applied in Agriculture

Cited by 39 publications

References 18 publications

Distinct Domains of CheA Confer Unique Functions in Chemotaxis and Cell Length in Azospirillum brasilense Sp7

Distinct Domains of CheA Confer Unique Functions in Chemotaxis and Cell Length in Azospirillum brasilense Sp7

Azospirillum brasilense Chemotaxis Depends on Two Signaling Pathways Regulating Distinct Motility Parameters

Cell–Cell Communication in Azospirillum and Related PGPR

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