Diversity and Evolution of Type III Secreted Effectors: A Case Study of Three Families

Bastedo, D. Patrick; Lo, Timothy; Laflamme, Bradley; Desveaux, Darrell; Guttman, David S.

doi:10.1007/82_2019_165

Cited by 15 publications

(16 citation statements)

References 154 publications

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“…The common "Sct" nomenclature 1,2 is used for T3SS components; when specifically referring to components of a particular species, the species initials are used as a prefix, e.g., YeSctD for Y. enterocolitica SctD. While the T3SS effectors differ among the different bacterial species 3,4 , and can have different functions in modulating the cytoskeleton, invading and escaping host cells or endosomes, or inducing host cell death (see reviews for animal pathogenic bacteria 1,[5][6][7][8][9][10] and T3SS-plant interactions 11 , the structural proteins of the injectisome are highly conserved 12,13 . An extracellular needle is formed by helical polymerization of a T3SS-exported protein, and ends in a pentameric tip structure.…”

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confidence: 99%

Dynamic relocalization of cytosolic type III secretion system components prevents premature protein secretion at low external pH

et al. 2021

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Many bacterial pathogens use a type III secretion system (T3SS) to manipulate host cells. Protein secretion by the T3SS injectisome is activated upon contact to any host cell, and it has been unclear how premature secretion is prevented during infection. Here we report that in the gastrointestinal pathogens Yersinia enterocolitica and Shigella flexneri, cytosolic injectisome components are temporarily released from the proximal interface of the injectisome at low external pH, preventing protein secretion in acidic environments, such as the stomach. We show that in Yersinia enterocolitica, low external pH is detected in the periplasm and leads to a partial dissociation of the inner membrane injectisome component SctD, which in turn causes the dissociation of the cytosolic T3SS components. This effect is reversed upon restoration of neutral pH, allowing a fast activation of the T3SS at the native target regions within the host. These findings indicate that the cytosolic components form an adaptive regulatory interface, which regulates T3SS activity in response to environmental conditions.

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Dynamic relocalization of cytosolic type III secretion system components prevents premature protein secretion at low external pH

et al. 2021

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“…93 Other evasion mechanisms, e.g., SCV membrane shielding of PAMPs from the cytosolic NAIPs, and active interference by secreted virulence factors, might further dampen residual inflammasome activation in a cell-type specific manner. 1,24 Also, it remains to be fully shown how polymerization into the flagellum affects the NAIP/NLRC4 triggering intensity of flagellin. Anyhow, the evasion of recognition is possibly already employed during IEC-invasion, but may be hampered by high bacterial invasion rates and relatively long lifetimes of the bacterial proteins.…”

Section: Discussionmentioning

confidence: 99%

“…For an adapted pathogen like S. Tm, this task is complicated by the bacterium's evolved ability to evade PRR recognition, through e.g., context-dependent regulation of its gene expression or inhibition of host-cell signaling. 1,24,25 Inflammasomes are multimeric signaling complexes that assemble in the host cell cytosol upon sensing of PAMPs or cellular damage by PRRs of the Nod-like receptor family (NLRs; NLRP1, NLRP3, NLRC4), Aim2, or Pyrin. 26 Inflammasome assembly causes cleavage of pro-inflammatory Caspase-1, 27 secretion of RESULTS NAIP/NLRC4 potently restricts S. Tm migration from the gut lumen to systemic sites Our in vivo analysis of the NAIP/NLRC4-mediated defense focused on the S. Tm infection dynamics during the first 24h after orogastric inoculation in the Streptomycin pretreated mouse model.…”

Section: Introductionmentioning

confidence: 99%

Intestinal epithelial NAIP/NLRC4 restricts systemic dissemination of the adapted pathogen Salmonella Typhimurium due to site-specific bacterial PAMP expression

et al. 2020

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Inflammasomes can prevent systemic dissemination of enteropathogenic bacteria. As adapted pathogens including Salmonella Typhimurium (S. Tm) have evolved evasion strategies, it has remained unclear when and where inflammasomes restrict their dissemination. Bacterial population dynamics establish that the NAIP/NLRC4 inflammasome specifically restricts S. Tm migration from the gut to draining lymph nodes. This is solely attributable to NAIP/NLRC4 within intestinal epithelial cells (IECs), while S. Tm evades restriction by phagocyte NAIP/NLRC4. NLRP3 and Caspase-11 also fail to restrict S. Tm mucosa traversal, migration to lymph nodes, and systemic pathogen growth. The ability of IECs (not phagocytes) to mount a NAIP/NLRC4 defense in vivo is explained by particularly high NAIP/NLRC4 expression in IECs and the necessity for epithelium-invading S. Tm to express the NAIP1-6 ligandsflagella and type-III-secretion-system-1. Imaging reveals both ligands to be promptly downregulated following IEC-traversal. These results highlight the importance of intestinal epithelial NAIP/NLRC4 in blocking bacterial dissemination in vivo, and explain why this constitutes a uniquely evasion-proof defense against the adapted enteropathogen S. Tm.Mucosal Immunology (2020) 13:530-544; https://doi.

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“…TALEs are numerous within Xoo and X. oryzae pv. oryzicola but few or even absent in other Xanthomonas species ( 49 ). This contrasting size of TALE repertoires is postulated as the result of different evolutionary forces acting on different Xanthomonas lineages ( 49 , 50 ).…”

Section: Discussionmentioning

confidence: 99%

Elucidation of the Pathogenicity-Associated Regulatory Network in Xanthomonas oryzae pv. oryzae

Zheng

Zhong

et al. 2021

mSystems

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Xanthomonas is a notorious plant pathogen causing serious diseases in hundreds of plant hosts. Xanthomonas species are equipped with an array of signal transduction systems that regulate gene expression to survive in various harsh environments and successfully infect hosts. Although certain pathogenicity-associated regulators have been functionally characterized, signal transduction systems always function as a regulatory network which remains to be elucidated in Xanthomonas. This study used a systematic approach to characterize all identified pathogenicity-associated regulators in Xanthomonas oryzae pv. oryzae (Xoo), including a transcriptional regulator with unknown function, and their interactive regulatory network. RNA sequencing was used in elucidating the patterns of the 10 pathogenicity-associated regulators identified. Results revealed that each pathogenicity-associated regulator has cross talk with others and all these regulators function as a regulatory network, with VemR and PXO_RS20790 being the master pathogenicity-associated regulators and HrpX being the final executant. Moreover, regulome analysis showed that numerous genes other than genes in pathogenicity islands are finely regulated within the regulatory network. Given that most of the pathogenicity-associated regulators are conserved in Xanthomonadales, our findings suggest a global network of gene regulation in this evolutionarily conserved pathogen. In conclusion, our study provides essential basic information about the regulatory network in Xoo, suggesting that this complicated regulatory network is one of the reasons for the robustness and fitness of Xanthomonas spp. IMPORTANCE The host plant infection process of pathogenic bacteria is a coordinating cellular behavior, which requires dynamic regulation at several levels in response to variations in host plants or fluctuations in the external environment. As one of the most important genera of plant-pathogenic bacteria, Xanthomonas has been studied as a model. Although certain pathogenicity-associated regulators have been functionally characterized, interactions among them remain to be elucidated. This study systematically characterized pathogenicity-associated regulators in Xoo and revealed that cross talk exists among pathogenicity-associated regulators and function as a regulatory network in which a hierarchy exists among the regulators. Our study elucidated the landscape of the pathogenicity-associated regulatory network in Xanthomonas, promoting understanding of the infection process of pathogenic bacteria.

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Diversity and Evolution of Type III Secreted Effectors: A Case Study of Three Families

Cited by 15 publications

References 154 publications

Dynamic relocalization of cytosolic type III secretion system components prevents premature protein secretion at low external pH

Dynamic relocalization of cytosolic type III secretion system components prevents premature protein secretion at low external pH

Intestinal epithelial NAIP/NLRC4 restricts systemic dissemination of the adapted pathogen Salmonella Typhimurium due to site-specific bacterial PAMP expression

Elucidation of the Pathogenicity-Associated Regulatory Network in Xanthomonas oryzae pv. oryzae

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