Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies

Sugawara, Masayuki; Epstein, Brendan; Badgley, Brian D.; Unno, Tatsuya; Lei, Xu; Reese, J. Luke; Gyaneshwar, Prasad; Denny, Roxanne; Mudge, Joann; Bharti, Arvind K.; Farmer, Andrew; May, Gregory D.; Woodward, Jimmy E.; Médigue, Claudine; Vallenet, David; Lajus, Aurélie; Rouy, Zoé; Martinez-Vaz, Betsy M.; Tiffin, Peter; Young, Nevin D.; Sadowsky, Michael J.

doi:10.1186/gb-2013-14-2-r17

Cited by 150 publications

(140 citation statements)

References 50 publications

(66 reference statements)

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“…2A). Similar to the findings of previous studies that conducted pangenome analyses (43,45,49), the highest number of core genes was observed in the functional category J (translation, ribosomal structure, and biogenesis). Furthermore, functional assignment based on COG classification revealed that most FIG 2 Pangenome analysis of Sulfobacillus strains.…”

Section: Figsupporting

confidence: 88%

“…S. thermosulfidooxidans Cutipay had the largest genome size (3.86 Mb) and number of CDSs (4,250), whereas S. thermosulfidooxidans DX had the smallest genome size (3.18 Mb) and number of CDSs (3,211). These findings indicated that numerous accessory genes in S. thermosulfidooxidans Cutipay were likely acquired by HGT, similar to earlier comparative genomic analyses of Sinorhizobium strains (45,46).…”

Section: Figsupporting

confidence: 84%

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Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

Zhang

Liu

Liang

et al. 2017

Appl Environ Microbiol

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Recent phylogenomic analysis has suggested that three strains isolated from different copper mine tailings around the world were taxonomically affiliated with Sulfobacillus thermosulfidooxidans. Here, we present a detailed investigation of their genomic features, particularly with respect to metabolic potentials and stress tolerance mechanisms. Comprehensive analysis of the Sulfobacillus genomes identified a core set of essential genes with specialized biological functions in the survival of acidophiles in their habitats, despite differences in their metabolic pathways. The Sulfobacillus strains also showed evidence for stress management, thereby enabling them to efficiently respond to harsh environments. Further analysis of metabolic profiles provided novel insights into the presence of genomic streamlining, highlighting the importance of gene loss as a main mechanism that potentially contributes to cellular economization. Another important evolutionary force, especially in larger genomes, is gene acquisition via horizontal gene transfer (HGT), which might play a crucial role in the recruitment of novel functionalities. Also, a successful integration of genes acquired from archaeal donors appears to be an effective way of enhancing the adaptive capacity to cope with environmental changes. Taken together, the findings of this study significantly expand the spectrum of HGT and genome reduction in shaping the evolutionary history of Sulfobacillus strains.IMPORTANCE Horizontal gene transfer (HGT) and gene loss are recognized as major driving forces that contribute to the adaptive evolution of microbial genomes, although their relative importance remains elusive. The findings of this study suggest that highly frequent gene turnovers within microorganisms via HGT were necessary to incur additional novel functionalities to increase the capacity of acidophiles to adapt to changing environments. Evidence also reveals a fascinating phenomenon of potential cross-kingdom HGT. Furthermore, genome streamlining may be a critical force in driving the evolution of microbial genomes. Taken together, this study provides insights into the importance of both HGT and gene loss in the evolution and diversification of bacterial genomes.

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Section: Figsupporting

confidence: 88%

Section: Figsupporting

confidence: 84%

Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

Zhang

Liu

Liang

et al. 2017

Appl Environ Microbiol

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“…syrM, nodD3, and syrA appear to be universal in the Sinorhizobium genus based on published genome sequences (95)(96)(97)(98)(99)(100)(101)(102)(103)(104). Among S. meliloti and S. medicae strains, the orthologous proteins are nearly identical, and the gene arrangement is syntenic to S. meliloti Rm1021 (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Rm1021 lacks functional genes encoding NolR, a nod gene repressor (109), ExpR, an LuxR-family global regulator of population-based behavior (6), EcfRI, which regulates sulfite metabolism (110), PstC, involved in high-affinity phosphate transport (111), and perhaps others (99,102). NolR of S. meliloti Rm41 represses expression of nodD1 and nodD2 but probably not nodD3 and syrM (112); NolR may also regulate genes involved in bacterial growth, survival, and conjugative plasmid transfer (113).…”

Section: Discussionmentioning

confidence: 99%

The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3

Barnett

Long

2015

J Bacteriol

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In Sinorhizobium meliloti, three NodD transcriptional regulators activate bacterial nodulation (nod) gene expression. NodD1 and NodD2 require plant compounds to activate nod genes. The NodD3 protein does not require exogenous compounds to activate nod gene expression; instead, another transcriptional regulator, SyrM, activates nodD3 expression. In addition, NodD3 can activate syrM expression. SyrM also activates expression of another gene, syrA, which when overexpressed causes a dramatic increase in exopolysaccharide production. In a previous study, we identified more than 200 genes with altered expression in a strain overexpressing nodD3. In this work, we define the transcriptomes of strains overexpressing syrM or syrA. The syrM, nodD3, and syrA overexpression transcriptomes share similar gene expression changes; analyses imply that nodD3 and syrA are the only targets directly activated by SyrM. We propose that most of the gene expression changes observed when nodD3 is overexpressed are due to NodD3 activation of syrM expression, which in turn stimulates SyrM activation of syrA expression. The subsequent increase in SyrA abundance results in broad changes in gene expression, most likely mediated by the ChvI-ExoS-ExoR regulatory circuit. IMPORTANCESymbioses with bacteria are prevalent across the animal and plant kingdoms. Our system of study, the rhizobium-legume symbiosis (Sinorhizobium meliloti and Medicago spp.), involves specific host-microbe signaling, differentiation in both partners, and metabolic exchange of bacterial fixed nitrogen for host photosynthate. During this complex developmental process, both bacteria and plants undergo profound changes in gene expression. The S. meliloti SyrM-NodD3-SyrA and ChvI-ExoS-ExoR regulatory circuits affect gene expression and are important for optimal symbiosis. In this study, we defined the transcriptomes of S. meliloti overexpressing SyrM or SyrA. In addition to identifying new targets of the SyrM-NodD3-SyrA regulatory circuit, our work further suggests how it is linked to the ChvI-ExoS-ExoR regulatory circuit. The symbiotic soil alphaproteobacterium Sinorhizobium meliloti forms nitrogen-fixing nodules on the roots of leguminous plants such as Medicago sativa (alfalfa) and Medicago truncatula (barrel medic). The earliest stages of the symbiosis involve an exchange of molecular signals: plant roots exude compounds that induce transcription of bacterial nod genes, which encode enzymes that synthesize lipochitooligosaccharide Nod factors (NF) (1, 2). These bacterial NF trigger early plant responses such as root hair curling, calcium spiking, and root cortical cell divisions to form the nodule organ (2). Bacteria trapped in curled root hairs penetrate the root hair through an infection thread (IT), an ingrowth of plant cell membrane and wall (3). As the IT elongates into the root, the bacteria at the tip are actively dividing.Bacterial polysaccharides, such as cyclic ␤-glucans and exopolysaccharide I (EPS-I; also known as succinoglycan), are essential for bacte...

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“…viciae population. This core value is similar in size to genetic cores found for other related species, such as Ensifer medicae (5,036 core genes for 12 genomes), E. fredii (5,979 core genes for 2 genomes) or E. meliloti (4,680 core genes for 32 genomes) (Sugawara et al, 2013). …”

Section: Exclusive Genes In Plant Host Mesocosm-selected Strainssupporting

confidence: 81%

Genomics of Specificity in the Symbiotic Interaction between Rhizobium leguminosarum and Legumes

Rubio¹

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. Para el desarrollo de esta Tesis he contado con una beca UPM homologada financiada por el proyecto MICROGEN: Genómica Comparada Microbiana (Programa Consolider), que ha sido también el proyecto financiador del trabajo experimental.Quisiera reconocer la labor de aquellas personas que han contribuido al desarrollo y consecución de esta Tesis.Dr. Juan Imperial, por la dirección y supervisión de esta Tesis. Por ser un gran mentor y por enseñarme todo lo que sé.Dr. Manuel González Guerrero, por enseñarme los entresijos de la Ciencia y del trabajo en el laboratorio.Dra. Gisèle Laguerre, por su participación en el inicio de este proyecto y por facilitarnos el suelo P1 de Dijon.Dr. Paulo Arruda, por la formación que obtuve durante mi estancia en el laboratorio de Estudio de la Regulación y de la Expresión génica de la Universidad Estatal de Campinas.Dra. Belén Brito, por su gran ayuda en la primera fase de este proyecto y por recomendarme, sin ella nunca hubiera empezado esta Tesis.Rosabel Prieto, por su inestimable ayuda para la obtención de los Pool-Seqs y por enseñarme muchas de las técnicas que he necesitado durante la Tesis.Santiago de la Peña, por su valiosa ayuda en el análisis bioinformático de los genomas individuales.Dra. Julia Quintana, por enseñarme los conceptos de genética de poblaciones y por las largas discusiones científicas que tanto me han aportado.Dra. Viviana Escudero, por enseñarme a cuidar las plantas y valorar las cosas realmente importantes. Dra. Carmen Sánchez, por enseñarme las técnicas básicas de microbiología y genética molecular durante mi periodo como estudiante de máster.Dr. David Durán, por enseñarme los conceptos básicos de filogenia. XIII AGRADECIMIENTOSEscribir los agradecimientos es la parte más difícil de una tesis, no porque sea complicado, si no porque es la única parte que se lee todo el mundo y supone una gran presión añadida. Siempre me imaginaba escribir esta parte como algo extremadamente emotivo, pero después de escribir más de 200 páginas me he quedado sin palabras.La ciencia siempre fue lo que quise hacer, pero nunca pensé que pudiera hacerlo, pero… here I am! Ha sido un camino largo y duro, pero no lo cambiaría por nada, me he convertido en lo que quería y he conocido a los mejores. Desde que tengo 13 años sabía que quería estudiar esto, gracias a la inspiración de mi profesora de biología Marisa Alonso. Cuando llegué a la carrera, las cosas no fueron como esperaba, pero aún así descubrí mi pasión por la micro, la genética y las plantas… Y sobre todo conocí a grandes personas. Desde luego la mejor decisión que tomé fue hacer el máster, este fue el punto de inflexión, descubrí que era hacer ciencia… y eso me enganchó. Quiero agradecer a Pepe Palacios por acogerme en su laboratorio durante este periodo, ya que sin duda, mi paso por allí marcó mi vuelta. Por ello también quiero agradecer a todos los Rizobios y Levaduros, y en especial a Carmen Sánchez, por ser mi supervisora en los inicios y enseñarme muchas de las técnicas básicas de micro y genética molecular que he apre...

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Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies

Cited by 150 publications

References 50 publications

Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

Adaptive Evolution of Extreme Acidophile Sulfobacillus thermosulfidooxidans Potentially Driven by Horizontal Gene Transfer and Gene Loss

The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3

Genomics of Specificity in the Symbiotic Interaction between Rhizobium leguminosarum and Legumes

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