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

Blanvillain, Servane; Meyer, Damien; Boulanger, Alice; Lautier, Martine; Guynet, Catherine; Denancé, Nicolás; Vasse, Jacques; Lauber, Emmanuelle; Arlat, Matthieu

doi:10.1371/journal.pone.0000224

Cited by 294 publications

(355 citation statements)

References 122 publications

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“…Therefore, the reduction in ability of the GAPDH-defective mutant to utilize available carbohydrates in the host reduces its growth, with consequences for its aggressiveness. Consistent with this, it has recently been demonstrated that glucose and sucrose utilization is required for full virulence in Xcc (Blanvillain et al, 2007;Lu et al, 2007b). Previously, we have shown that an Xcc ppsA (a gene encoding phosphoenolpyruvate synthase, the key enzyme in gluconeogenesis) mutant, which has lost the capability to utilize pyruvate and C 4 dicarboxylates as carbon sources, has limited growth in host tissues and significantly reduced virulence compared with the wildtype .…”

Section: Discussionsupporting

confidence: 78%

Glyceraldehyde-3-phosphate dehydrogenase of Xanthomonas campestris pv. campestris is required for extracellular polysaccharide production and full virulence

Lu¹,

Xie²,

Chen³

et al. 2009

Microbiology

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Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) plays an important role in glucose catabolism, converting glyceraldehyde 3-phosphates to 1,3-bisphosphoglycerates. Open reading frame (ORF) XC_0972 in the genome of Xanthomonas campestris pv. campestris (Xcc) strain 8004 is the only ORF in this strain annotated to encode a GAPDH. In this work, we have demonstrated genetically that this ORF encodes a unique GAPDH in Xcc strain 8004, which seems to be constitutively expressed. A GAPDH-deficient mutant could still grow in medium with glucose or other sugars as the sole carbon source, and no phosphofructokinase activity was detectable in strain 8004. These facts suggest that Xcc may employ the Entner-Doudoroff pathway, but not glycolysis, to utilize glucose. The mutant could not utilize pyruvate as sole carbon source, whereas the wild-type could, implying that the GAPDH of Xcc is involved in gluconeogenesis. Furthermore, inactivation of the Xcc GAPDH resulted in impairment of bacterial growth and virulence in the host plant, and reduction of intracellular ATP and extracellular polysaccharide (EPS). This reveals that GAPDH is required for EPS production and full pathogenicity of Xcc.

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Section: Discussionsupporting

confidence: 78%

Glyceraldehyde-3-phosphate dehydrogenase of Xanthomonas campestris pv. campestris is required for extracellular polysaccharide production and full virulence

Lu¹,

Xie²,

Chen³

et al. 2009

Microbiology

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“…XCC3358 was recently described as one of 72 TonB-dependent receptors in the phytopathogen Xanthomonas campestris pv. campestris (Xcc) transporting sucrose with high affinity, and found to be required for full pathogenicity on Arabidopsis (26). Overall, the presence of multiple TonB transporters may account for the large abundance of Sphingomonas spp.…”

Section: Plant-associated Lifestylementioning

confidence: 99%

Community proteogenomics reveals insights into the physiology of phyllosphere bacteria

Delmotte

Knief

Chaffron

et al. 2009

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

773

656

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Aerial plant surfaces represent the largest biological interface on Earth and provide essential services as sites of carbon dioxide fixation, molecular oxygen release, and primary biomass production. Rather than existing as axenic organisms, plants are colonized by microorganisms that affect both their health and growth. To gain insight into the physiology of phyllosphere bacteria under in situ conditions, we performed a culture-independent analysis of the microbiota associated with leaves of soybean, clover, and Arabidopsis thaliana plants using a metaproteogenomic approach. We found a high consistency of the communities on the 3 different plant species, both with respect to the predominant community members (including the alphaproteobacterial genera Sphingomonas and Methylobacterium) and with respect to their proteomes. Observed known proteins of Methylobacterium were to a large extent related to the ability of these bacteria to use methanol as a source of carbon and energy. A remarkably high expression of various TonB-dependent receptors was observed for Sphingomonas. Because these outer membrane proteins are involved in transport processes of various carbohydrates, a particularly large substrate utilization pattern for Sphingomonads can be assumed to occur in the phyllosphere. These adaptations at the genus level can be expected to contribute to the success and coexistence of these 2 taxa on plant leaves. We anticipate that our results will form the basis for the identification of unique traits of phyllosphere bacteria, and for uncovering previously unrecorded mechanisms of bacteria-plant and bacteria-bacteria relationships.metaproteomics ͉ methylotrophy ͉ plant phyllosphere ͉ Pseudomonas ͉ Sphingomonas F or terrestrial plants, the phyllosphere represents the interface between the above-ground parts of plants and the air. Conservative estimates indicate that the roughly 1 billion square kilometers of worldwide leaf surfaces host more than 10 26 bacteria, which are the most abundant colonizers of this habitat (1, 2). The overall microbiota in this ecosystem is thus sufficiently large to have an impact on the global carbon and nitrogen cycles. Additionally, the phyllosphere inhabitants influence their hosts at the level of the individual plants. To a large extent, interest in phyllosphere microbiology has been driven by investigations on plant pathogens. Their spread, colonization, survival, and pathogenicity mechanisms have been the subject of numerous studies (2). Much less understood are nonpathogenic microorganisms that inhabit the phyllosphere. The composition of the phyllosphere microbiota has been analyzed in only a few studies by cultivation-independent methods (e.g., refs. 3-5); however, such methods are essential in light of the yet uncultivated majority of bacteria existing in nature (6), or more specifically on plant leaves (7). Not only their identity, but in particular the physiological properties of phyllosphere bacteria, their adaptations to the habitat, and their potential role (e.g., with res...

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“…TonBdependent channels were originally identified in the context of iron transport, but have since been associated with the transport of a large variety of compounds (Schauer et al, 2008). Of particular interest is their newly recognized association with degradation of polymers and complex carbohydrates (Blanvillain et al, 2007;Martens et al, 2009). Several of the TonB-dependent channels in Polaribacter sp, MED152 were associated with predicted peptidases and glycosyl hydrolases (González et al, 2008), suggesting they may be involved in utilization of high molecular weight substrates in this organism.…”

Section: Nutrient Acquisition Strategies Of Monterey Bay Rhodobacteramentioning

confidence: 99%

Metatranscriptomic analysis of autonomously collected and preserved marine bacterioplankton

et al. 2011

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Planktonic microbial activity and community structure is dynamic, and can change dramatically on time scales of hours to days. Yet for logistical reasons, this temporal scale is typically undersampled in the marine environment. In order to facilitate higher-resolution, long-term observation of microbial diversity and activity, we developed a protocol for automated collection and fixation of marine microbes using the Environmental Sample Processor (ESP) platform. The protocol applies a preservative (RNALater) to cells collected on filters, for long-term storage and preservation of total cellular RNA. Microbial samples preserved using this protocol yielded high-quality RNA after 30 days of storage at room temperature, or onboard the ESP at in situ temperatures. Pyrosequencing of complementary DNA libraries generated from ESP-collected and preserved samples yielded transcript abundance profiles nearly indistinguishable from those derived from conventionally treated replicate samples. To demonstrate the utility of the method, we used a moored ESP to remotely and autonomously collect Monterey Bay seawater for metatranscriptomic analysis. Community RNA was extracted and pyrosequenced from samples collected at four time points over the course of a single day. In all four samples, the oxygenic photoautotrophs were predominantly eukaryotic, while the bacterial community was dominated by Polaribacter-like Flavobacteria and a Rhodobacterales bacterium sharing high similarity with Rhodobacterales sp. HTCC2255. However, each time point was associated with distinct species abundance and gene transcript profiles. These laboratory and field tests confirmed that autonomous collection and preservation is a feasible and useful approach for characterizing the expressed genes and environmental responses of marine microbial communities.

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

Cited by 294 publications

References 122 publications

Glyceraldehyde-3-phosphate dehydrogenase of Xanthomonas campestris pv. campestris is required for extracellular polysaccharide production and full virulence

Glyceraldehyde-3-phosphate dehydrogenase of Xanthomonas campestris pv. campestris is required for extracellular polysaccharide production and full virulence

Community proteogenomics reveals insights into the physiology of phyllosphere bacteria

Metatranscriptomic analysis of autonomously collected and preserved marine bacterioplankton

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