Plant Carbohydrate Scavenging through TonB-Dependent Receptors: A Feature Shared by Phytopathogenic and Aquatic Bacteria

TonB-dependent receptors (TBDRs) are outer membrane proteins mainly known for the active transport of iron siderophore complexes in Gram-negative bacteria. Analysis of the genome of the phytopathogenic bacterium Xanthomonas campestris pv. campestris (Xcc), predicts 72 TBDRs. Such an overrepresentation is common in Xanthomonas species but is limited to only a small number of bacteria. Here, we show that one Xcc TBDR transports sucrose with a very high affinity, suggesting that it might be a sucrose scavenger. This TBDR acts with an inner membrane transporter, an amylosucrase and a regulator to utilize sucrose, thus defining a new type of carbohydrate utilization locus, named CUT locus, involving a TBDR for the transport of substrate across the outer membrane. This sucrose CUT locus is required for full pathogenicity on Arabidopsis, showing its importance for the adaptation to host plants. A systematic analysis of Xcc TBDR genes and a genome context survey suggested that several Xcc TBDRs belong to other CUT loci involved in the utilization of various plant carbohydrates. Interestingly, several Xcc TBDRs and CUT loci are conserved in aquatic bacteria such as Caulobacter crescentus, Colwellia psychrerythraea, Saccharophagus degradans, Shewanella spp., Sphingomonas spp. or Pseudoalteromonas spp., which share the ability to degrade a wide variety of complex carbohydrates and display TBDR overrepresentation. We therefore propose that TBDR overrepresentation and the presence of CUT loci designate the ability to scavenge carbohydrates. Thus CUT loci, which seem to participate to the adaptation of phytopathogenic bacteria to their host plants, might also play a very important role in the biogeochemical cycling of plant-derived nutrients in marine environments. Moreover, the TBDRs and CUT loci identified in this study are clearly different from those characterized in the human gut symbiont Bacteroides thetaiotaomicron, which allow glycan foraging, suggesting a convergent evolution of TBDRs in Proteobacteria and Bacteroidetes

The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae

<p>Abstract</p> <p>Background</p> <p>The <it>Xanthomonadaceae </it>family contains two xylem-limited plant pathogenic bacterial species, <it>Xanthomonas albilineans </it>and <it>Xylella fastidiosa</it>. <it>X. fastidiosa </it>was the first completely sequenced plant pathogen. It is insect-vectored, has a reduced genome and does not possess <it>hrp </it>genes which encode a Type III secretion system found in most plant pathogenic bacteria. <it>X. fastidiosa </it>was excluded from the <it>Xanthomonas </it>group based on phylogenetic analyses with rRNA sequences.</p> <p>Results</p> <p>The complete genome of <it>X. albilineans </it>was sequenced and annotated. <it>X. albilineans</it>, which is not known to be insect-vectored, also has a reduced genome and does not possess <it>hrp </it>genes. Phylogenetic analysis using <it>X. albilineans </it>genomic sequences showed that <it>X. fastidiosa </it>belongs to the <it>Xanthomonas </it>group. Order of divergence of the <it>Xanthomonadaceae </it>revealed that <it>X. albilineans </it>and <it>X. fastidiosa </it>experienced a convergent reductive genome evolution during their descent from the progenitor of the <it>Xanthomonas </it>genus. Reductive genome evolutions of the two xylem-limited <it>Xanthomonadaceae </it>were compared in light of their genome characteristics and those of obligate animal symbionts and pathogens.</p> <p>Conclusion</p> <p>The two xylem-limited <it>Xanthomonadaceae</it>, during their descent from a common ancestral parent, experienced a convergent reductive genome evolution. Adaptation to the nutrient-poor xylem elements and to the cloistered environmental niche of xylem vessels probably favoured this convergent evolution. However, genome characteristics of <it>X. albilineans </it>differ from those of <it>X. fastidiosa </it>and obligate animal symbionts and pathogens, indicating that a distinctive process was responsible for the reductive genome evolution in this pathogen. The possible role in genome reduction of the unique toxin albicidin, produced by <it>X. albilineans</it>, is discussed.</p

Genome sequencing of Xanthomonas axonopodis pv. phaseoli CFBP4834-R reveals that flagellar motility is not a general feature of xanthomonads.

Xanthomonads are plant-associated bacteria that establish neutral, commensal or pathogenic relationships with plants. The list of common characteristics shared by all members of the genus Xanthomonas is now well established based on the entire genome sequences that are currently available and that represent various species, numerous pathovars of X. axonopodis (sensu Vauterin et al., 2000), X. oryzae and X. campestris, and many strains within some pathovars. These ?-proteobacteria are motile by a single polar flagellum. Motility is an important feature involved in biofilm formation, plant colonization and hence considered as a pathogenicity factor. X. axonopodis pv. phaseoli var. fuscans (Xapf) is one of the causal agents of common bacterial blight of bean and 4834-R is a highly aggressive strain of this pathogen that was isolated from a seed-borne epidemic in France in 1998. We obtained a high quality assembled sequence of the genome of this strain with 454-Solexa and 2X Sanger sequencing. Housekeeping functions are conserved in this genome that shares core characteristics with genomes of other xanthomonads: the six secretion systems which have been described so far in Gram negative bacteria are all present, as well as their ubiquitous substrates or effectors and a rather usual number of mobile elements. Elements devoted to the adaptation to the environment constitute an important part of the genome with a chemotaxis island and dispersed MCPs, numerous two-component systems, and numerous TonB dependent transporters. Furthermore, numerous multidrug efflux systems and functions dedicated to biofilm formation that confer resistance to stresses are also present. An intriguing feature revealed by genome analysis is a long deletion of 35 genes (33 kbp) involved in flagellar biosynthesis. This deletion is replaced by an insertion sequence called ISXapf2. Genes such as flgB to flgL and fliC to fleQ which are involved in the flagellar structure (rod, P- and L-ring, hook, cap and filament) are absent in the genome of strain 4834-R that is not motile. Primers were designed to detect this deletion by PCR in a collection of more than 300 strains representing different species and pathovars of Xanthomonas, and less than 5% of the tested xanthomonads strains were found nonmotile because of a deletion in the flagellum gene cluster. We observed that half of the Xapf strains isolated from the same epidemic than strain 4834-R was non-motile and that this ratio was conserved in the strains colonizing the next bean seed generation. Isolation of such variants in a natural epidemic reveals that either flagellar motility is not a key function for fitness or that some complementation occurs within the bacterial population. (Résumé d'auteur

Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads

Abstract\ud \ud \ud \ud Background\ud Xanthomonads are plant-associated bacteria responsible for diseases on economically important crops. Xanthomonas fuscans subsp. fuscans (Xff) is one of the causal agents of common bacterial blight of bean. In this study, the complete genome sequence of strain Xff 4834-R was determined and compared to other Xanthomonas genome sequences.\ud \ud \ud \ud Results\ud Comparative genomics analyses revealed core characteristics shared between Xff 4834-R and other xanthomonads including chemotaxis elements, two-component systems, TonB-dependent transporters, secretion systems (from T1SS to T6SS) and multiple effectors. For instance a repertoire of 29 Type 3 Effectors (T3Es) with two Transcription Activator-Like Effectors was predicted. Mobile elements were associated with major modifications in the genome structure and gene content in comparison to other Xanthomonas genomes. Notably, a deletion of 33 kbp affects flagellum biosynthesis in Xff 4834-R. The presence of a complete flagellar cluster was assessed in a collection of more than 300 strains representing different species and pathovars of Xanthomonas. Five percent of the tested strains presented a deletion in the flagellar cluster and were non-motile. Moreover, half of the Xff strains isolated from the same epidemic than 4834-R was non-motile and this ratio was conserved in the strains colonizing the next bean seed generations.\ud \ud \ud \ud Conclusions\ud This work describes the first genome of a Xanthomonas strain pathogenic on bean and reports the existence of non-motile xanthomonads belonging to different species and pathovars. Isolation of such Xff variants from a natural epidemic may suggest that flagellar motility is not a key function for in planta fitness.AI is funded by a PhD grant from INRA-SPE and region Pays de la Loire, France. EG was funded by a PhD grant from the French Ministry of National Education and Research and French Guyana. SC, EG, MA, EL and LDN are funded by the LABEX TULIP (ANR-10-LABX-41), LSG is funded by ANR-2010-GENM-013 Xanthomix

Etudes des récepteurs TonB-dépendants et d'un nouvel effecteur de type III de la bactérie phytopathogène Xanthomonas campestris pv. campestris

TOULOUSE3-BU Sciences (315552104) / SudocSudocFranceF

Etude de la virulence et du régulome de la bactérie phytopathogène Xanthomonas campestris pv. campestris

TOULOUSE3-BU Sciences (315552104) / SudocSudocFranceF

Etude de la virulence et du régulome de la bactérie phytopathogène Xanthomonas campestris pv. campestris

TOULOUSE3-BU Sciences (315552104) / SudocSudocFranceF

From effectors to effectomes: Are functional studies of individual effectors enough to decipher plant pathogen infectious strategies?

International audienceEffector proteins of plant pathogens are key virulence determinants which can be secreted in the apoplast or translocated inside plant cells where they subvert host immunity and physiology to the pathogen's benefit [1]. In some specific plant accessions, effector proteins may also be detected by plant immune receptors and trigger strong specific resistance [2-4]