The Agrobacterium tumefaciens CheY-like protein ClaR regulates biofilm formation

Feirer, Nathan; Kim, DohHyun; Xu, Jing; Fernandez, Nico; Waters, Christopher M.; Fuqua, Clay

doi:10.1099/mic.0.000558

Cited by 13 publications

(14 citation statements)

References 77 publications

(99 reference statements)

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“…The genes encoding these DGCs were amplified and cloned under the control of the IPTG‐inducible lac promoter in the pTrc200 vector. Using agar plates‐containing Congo red, it is possible to reveal exopolysaccharide (EPS) production in response of increased intracellular levels of c‐di‐GMP (Howie and Brewer, ; Heckel et al , ; Heindl et al , ; Feirer et al , ; Feirer et al , ). It was clear that some of the A. tumefaciens transformed with the above recombinant plasmids yielded colonies displaying a wrinkly phenotype (Fig.…”

Section: Resultsmentioning

confidence: 99%

Cyclic di‐GMP inactivates T6SS and T4SS activity in Agrobacterium tumefaciens

McCarthy

Eilers

et al. 2019

Molecular Microbiology

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Summary The Type VI secretion system (T6SS) is a bacterial nanomachine that delivers effector proteins into prokaryotic and eukaryotic preys. This secretion system has emerged as a key player in regulating the microbial diversity in a population. In the plant pathogen Agrobacterium tumefaciens, the signalling cascades regulating the activity of this secretion system are poorly understood. Here, we outline how the universal eubacterial second messenger cyclic di‐GMP impacts the production of T6SS toxins and T6SS structural components. We demonstrate that this has a significant impact on the ability of the phytopathogen to compete with other bacterial species in vitro and in planta. Our results suggest that, as opposed to other bacteria, c‐di‐GMP turns down the T6SS in A. tumefaciens thus impacting its ability to compete with other bacterial species within the rhizosphere. We also demonstrate that elevated levels of c‐di‐GMP within the cell decrease the activity of the Type IV secretion system (T4SS) and subsequently the capacity of A. tumefaciens to transform plant cells. We propose that such peculiar control reflects on c‐di‐GMP being a key second messenger that silences energy‐costing systems during early colonization phase and biofilm formation, while low c‐di‐GMP levels unleash T6SS and T4SS to advance plant colonization.

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Section: Resultsmentioning

confidence: 99%

Cyclic di‐GMP inactivates T6SS and T4SS activity in Agrobacterium tumefaciens

McCarthy

Eilers

et al. 2019

Molecular Microbiology

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“…In the literature, the involvement of the flagellum during the attachment step is well documented, whereas a possible role of the chemotaxis regulator CheY has been poorly studied [48][49][50] . However, the involvement of Che or Che-like systems in building biofilms has been reported several times [51][52][53][54][55][56][57] . The fact that orthologous CheY proteins can suppress the defect of biofilm synthesis in a cheY3 mutant suggests a probable dual role of CheY in other bacteria.…”

Section: Discussionmentioning

confidence: 99%

The phosphorylated regulator of chemotaxis is crucial throughout biofilm biogenesis in Shewanella oneidensis

Boyeldieu¹,

Chaouche²,

Ba³

et al. 2020

npj Biofilms Microbiomes

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The core of the chemotaxis system of Shewanella oneidensis is made of the CheA3 kinase and the CheY3 regulator. When appropriated, CheA3 phosphorylates CheY3, which, in turn, binds to the rotor of the flagellum to modify the swimming direction. In this study, we showed that phosphorylated CheY3 (CheY3-P) also plays an essential role during biogenesis of the solid-surface-associated biofilm (SSA-biofilm). Indeed, in a ΔcheY3 strain, the formation of this biofilm is abolished. Using the phospho-mimetic CheY3D56E mutant, we showed that CheY-P is required throughout the biogenesis of the biofilm but CheY3 phosphorylation is independent of CheA3 during this process. We have recently found that CheY3 interacts with two diguanylate cyclases (DGCs) and with MxdA, the c-di-GMP effector, probably triggering exopolysaccharide synthesis by the Mxd machinery. Here, we discovered two additional DGCs involved in SSA-biofilm development and showed that one of them interacts with CheY3. We therefore propose that CheY3-P acts together with DGCs to control SSA-biofilm formation. Interestingly, two orthologous CheY regulators complement the biofilm defect of a ΔcheY3 strain, supporting the idea that biofilm formation could involve CheY regulators in other bacteria.

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“…This effect can be observed as a lack of binding to surfaces, and hence a lack of biofilm production (Xu et al 2012; Xu et al 2013). Consistent with its role in attachment, mutations which cause UPP overproduction greatly enhance attachment and biofilm formation (Feirer et al 2015; Feirer et al 2017; Wang et al 2014; Xu et al 2013).…”

Section: Exopolysaccharidesmentioning

confidence: 99%

Function and Regulation of Agrobacterium tumefaciens Cell Surface Structures that Promote Attachment

Thompson

Onyeziri

Fuqua

2018

Current Topics in Microbiology and Immunology

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Agrobacterium tumefaciens attaches stably to plant host tissues and abiotic surfaces. During pathogenesis, physical attachment to the site of infection is a prerequisite to infection and horizontal gene transfer to the plant. Virulent and avirulent strains may also attach to plant tissue in more benign plant associations, and as with other soil microbes, to soil surfaces in the terrestrial environment. Although most A. tumefaciens virulence functions are encoded on the tumor-inducing plasmid, genes that direct general surface attachment are chromosomally encoded, and thus this process is not obligatorily tied to virulence, but is a more fundamental capacity. Several different cellular structures are known or suspected to contribute to the attachment process. The flagella influence surface attachment primarily via their propulsive activity, but control of their rotation during the transition to the attached state may be quite complex. A. tumefaciens produces several pili, including the Tad-type Ctp pili, and several plasmid-borne conjugal pili encoded by the Ti and At plasmids, as well as the so-called T-pilus, involved in interkingdom horizontal gene transfer. The Ctp pili promote reversible interactions with surfaces, whereas the conjugal and T-pili drive horizontal gene transfer (HGT) interactions with other cells and tissues. The T-pilus is likely to contribute to physical association with plant tissues during DNA transfer to plants. A. tumefaciens can synthesize a variety of polysaccharides including cellulose, curdlan (β-1,3 glucan), β-1,2 glucan (cyclic and linear), succinoglycan, and a localized polysaccharide(s) that is confined to a single cellular pole and is called the unipolar polysaccharide (UPP). Lipopolysaccharides are also in the outer leaflet of the outer membrane. Cellulose and curdlan production can influence attachment under certain conditions. The UPP is required for stable attachment under a range of conditions and on abiotic and biotic surfaces. Other factors that have been reported to play a role in attachment include the elusive protein called rhicadhesin. The process of surface attachment is under extensive regulatory control and can be modulated by environmental conditions, as well as by direct responses to surface contact. Complex transcriptional and post-transcriptional control circuitry underlies much of the production and deployment of these attachment functions.

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The Agrobacterium tumefaciens CheY-like protein ClaR regulates biofilm formation

Cited by 13 publications

References 77 publications

Cyclic di‐GMP inactivates T6SS and T4SS activity in Agrobacterium tumefaciens

Cyclic di‐GMP inactivates T6SS and T4SS activity in Agrobacterium tumefaciens

The phosphorylated regulator of chemotaxis is crucial throughout biofilm biogenesis in Shewanella oneidensis

Function and Regulation of Agrobacterium tumefaciens Cell Surface Structures that Promote Attachment

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