Recipient Cell Factors Influence Interbacterial Competition Mediated by Two Distinct Burkholderia dolosa Contact-Dependent Growth Inhibition Systems

Elery, Zaria K.; Oates, Angela; Myers-Morales, Tanya; Garcia, Erin C.

doi:10.1128/jb.00541-21

Cited by 2 publications

(2 citation statements)

References 46 publications

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“…Bacterial mutants were marked with antibiotic resistance cassettes by att Tn7 delivery of pUC18Tmini-Tn-Kan ( 34 ), pUCTet ( 10 ), or for Bm CGD2M only, pUCCm (pMA41) ( 10 ). Markers were delivered via triparental matings of E. coli RHO3 with helper plasmid pTNS3, as previously described ( 35 , 36 ).…”

Section: Methodsmentioning

confidence: 99%

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Relaxed specificity of BcpB transporters mediates interactions between Burkholderia cepacia complex contact-dependent growth inhibition systems

Elery

Myers-Morales

Phillips

et al. 2023

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Belonging to the two-partner secretion family of proteins, contact-dependent growth inhibition (CDI) systems mediate interbacterial antagonism among closely related Gram-negative bacteria. The toxic portion of a large surface protein, BcpA/CdiA, is delivered to the cytoplasm of neighboring cells where it inhibits growth. Translocation of the antibacterial polypeptide out of the producing cell requires an associated outer membrane transporter, BcpB/CdiB. Some bacteria, including many Burkholderia species, encode multiple distinct CDI systems, but whether there is interaction between these systems is largely unknown. Using Burkholderia cepacia complex species as a model, here we show that related BcpB transporters exhibit considerable secretion flexibility and can secrete both cognate and non-cognate BcpA substrates. We also identified an additional unique Burkholderia dolosa CDI system capable of mediating interbacterial competition and demonstrated that its BcpB transporter has similar relaxed substrate specificity. Our results showed that two BcpB transporters (BcpB-2 and BcpB-3) were able to secrete all four of the B. dolosa BcpA toxins, while one transporter (BcpB-1) appeared unable to secrete even its cognate BcpA substrate under the tested conditions. This flexibility provided a competitive advantage, as strains lacking the full repertoire of BcpB proteins had decreased CDI activity. Similar results were obtained in Burkholderia multivorans , suggesting that secretion flexibility may be a conserved feature of Burkholderia CDI systems. Together these findings suggest that the interaction between distinct CDI systems enhances the efficiency of bacterial antagonism. IMPORTANCE The Burkholderia cepacia complex (Bcc) is a group of related opportunistic bacterial pathogens that occupy a diverse range of ecological niches and exacerbate disease in patients with underlying conditions. Contact-dependent growth inhibition (CDI) system proteins, produced by Gram-negative bacteria, contain antagonistic properties that allow for intoxication of closely related neighboring bacteria via a secreted protein, BcpA. Multiple unique CDI systems can be found in the same bacterial strain, and here we show that these distinct systems interact in several Bcc species. Our findings suggest that the interaction between CDI system proteins is important for interbacterial toxicity. Understanding the mechanism of interplay between CDI systems provides further insight into the complexity of bacterial antagonism. Moreover, since many bacterial species are predicted to encode multiple CDI systems, this study suggests that interactions between these distinct systems likely contribute to the overall competitive fitness of these species.

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Section: Methodsmentioning

confidence: 99%

“…Interbacterial competition assays were performed as previously described ( 36 ). B. dolosa or B. multivorans strains carrying antibiotic resistance cassettes at att Tn7 sites were cultured overnight without antibiotics and resuspended in sterile PBS to an OD 600 = 2.…”

Section: Methodsmentioning

confidence: 99%

Relaxed specificity of BcpB transporters mediates interactions between Burkholderia cepacia complex contact-dependent growth inhibition systems

Elery

Myers-Morales

Phillips

et al. 2023

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BglaTNB6, a tailocin produced by a plant-associated nonpathogenic bacterium, prevents rice seed-borne bacterial diseases

Kouzai,

Sagehashi,

Watanabe

et al. 2024

PLoS Pathog

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Rice seed-borne diseases caused by the bacterial pathogens Burkholderia glumae and B. plantarii pose a major threat to rice production worldwide. To manage these diseases in a sustainable manner, a biocontrol strategy is crucial. In this study, we showed that B. gladioli NB6 (NB6), a nonpathogenic bacterium, strongly protects rice from infection caused by the above-mentioned pathogens. NB6 was isolated from the indica rice cultivar Nona Bokra seedlings, which possesses genetic resistance to B. glumae. We discovered that cell suspensions of NB6 and its culture filtrate suppressed the disease symptoms caused by B. glumae and B. plantarii in rice seedlings, which indicated that NB6 secretes a plant-protective substance extracellularly. Through purification and mass spectrometry analysis of the culture filtrate, combined with transmission electron microscopy and mutant analysis, the substance was identified as a tailocin and named BglaTNB6. Tailocins are bacteriotoxic multiprotein structures morphologically similar to headless phage tails. BglaTNB6 exhibited antibacterial activity against several Burkholderia species, including B. glumae, B. plantarii, and B. gladioli, suggesting it can prevent pathogen infection. Interestingly, BglaTNB6 greatly contributed only to the biocontrol activity of NB6 cell suspensions against B. plantarii, and not against B. glumae. BglaTNB6 was shown to be encoded by a prophage locus lacking genes for phage head proteins, and a B. gladioli strain with the coded BglaTNB6-like locus equipped with phage head proteins failed to prevent rice seedlings from being infected with B. plantarii. These results suggested that BglaTNB6 may enhance the competitiveness of NB6 against a specific range of bacteria. Our study also highlights the potential of tailocin-producing endophytes for managing crop bacterial diseases.

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Recipient Cell Factors Influence Interbacterial Competition Mediated by Two Distinct Burkholderia dolosa Contact-Dependent Growth Inhibition Systems

Cited by 2 publications

References 46 publications

Relaxed specificity of BcpB transporters mediates interactions between Burkholderia cepacia complex contact-dependent growth inhibition systems

Relaxed specificity of BcpB transporters mediates interactions between Burkholderia cepacia complex contact-dependent growth inhibition systems

BglaTNB6, a tailocin produced by a plant-associated nonpathogenic bacterium, prevents rice seed-borne bacterial diseases

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