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Novel Components of the Flagellar System in Epsilonproteobacteria Mbio.Asm.Org Downloaded from RESEARCH ARTICLE Novel Components of the Flagellar System in Epsilonproteobacteria mbio.asm.org Beile Gao,a Maria Lara-Tejero,a Matthew Lefebre,a Andrew L. Goodman,a,b Jorge E. Galána Department of Microbial Pathogenesis, Yale University School of Medicine, New Haven, Connecticut, USAa; Microbial Diversity Institute, Yale University School of on August 16, 2016 - Published by Medicine, New Haven, Connecticut, USAb ABSTRACT Motility is essential for the pathogenesis of many bacterial species. Most bacteria move using flagella, which are multi- protein filaments that rotate propelled by a cell wall-anchored motor using chemical energy. Although some components of the flagellar apparatus are common to many bacterial species, recent studies have shown significant differences in the flagellar struc- tures of different bacterial species. The molecular bases for these differences, however, are not understood. The flagella from epsilonproteobacteria, which include the bacterial pathogens Campylobacter jejuni and Helicobacter pylori, are among the most divergent. Using next-generation sequencing combined with transposon mutagenesis, we have conducted a comprehensive high- throughput genetic screen in Campylobacter jejuni, which identified several novel components of its flagellar system. Biochemi- cal analyses detected interactions between the identified proteins and known components of the flagellar machinery, and in vivo imaging located them to the bacterial poles, where flagella assemble. Most of the identified new components are conserved mbio.asm.org within but restricted to epsilonproteobacteria. These studies provide insight into the divergent flagella of this group of bacteria and highlight the complexity of this remarkable structure, which has adapted to carry out its conserved functions in the context of widely diverse bacterial species. IMPORTANCE Motility is essential for the normal physiology and pathogenesis of many bacterial species. Most bacteria move us- ing flagella, which are multiprotein filaments that rotate propelled by a motor that uses chemical energy as fuel. Although some components of the flagellar apparatus are common to many bacterial species, recent studies have shown significant divergence in the flagellar structures across bacterial species. However, the molecular bases for these differences are not understood. The fla- gella from epsilonproteobacteria, which include the bacterial pathogens Campylobacter jejuni and Helicobacter pylori, are among the most divergent. We conducted a comprehensive genetic screen in Campylobacter jejuni and identified several novel components of the flagellar system. These studies provide important information to understand how flagella have adapted to function in the context of widely diverse sets of bacterial species and bring unique insight into the evolution and function of this remarkable bacterial organelle. Received 17 May 2014 Accepted 2 June 2014 Published 24 June 2014 Citation Gao B, Lara-Tejero M, Lefebre M, Goodman AL, Galán JE. 2014. Novel components of the flagellar system in epsilonproteobacteria. mBio 5(3):e01349-14. doi:10.1128/ mBio.01349-14. Editor Martin Blaser, New York University Copyright © 2014 Gao et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Address correspondence to Jorge E. Galán, [email protected]. he bacterial flagellum is a very complex nanomachine that is appropriate environment (3). Although the general organization Thighly conserved across bacterial species (1–3). Despite this of flagella is highly conserved, it has recently become apparent that conservation, there is significant variation in the numbers and the there is considerable diversity in the flagellar structure itself across locations of flagella on the bacterial body (4). While some bacteria bacterial species (1, 10, 11). In particular, cryo-electron tomogra- have multiple peritrichous flagella, others have a single flagellum phy studies have shown that flagella from members of the Epsilon- at one (unipolar or monotrichous) or both (bipolar or amphi- proteobacteria are among the most structurally diverse, exhibiting trichous) poles or have flagella embedded within the periplasmic several unique structural features that most likely correspond to space (5–8). Numerous studies, mostly carried out in the model novel, yet unidentified, flagellar components (12). Understanding organisms Salmonella enterica serovar Typhimurium and Esche- the molecular bases for these differences would be important to richia coli, have provided detailed information about the compo- understand the evolution and adaptation of this bacterial organ- sition, structure, assembly, and function of this remarkable organ- elle across bacterial species. elle (3, 9). These studies have shown that the bacterial flagellum All members of the Epsilonproteobacteria have their flagella lo- consists of two main structural components, the hook basal body cated at either one or both cellular poles (13–19). Campylobacter complex and the extracellular filament. In addition, a number of jejuni and Helicobacter pylori are the most studied epsilonproteo- nonstructural components are required for flagellar assembly and bacteria because they are important human pathogens. C. jejuni is function. The deployment of the flagellar apparatus is highly reg- a major cause of food-borne illness (20, 21), while H. pylori is an ulated by a complex regulatory network that ensures the expres- important cause of stomach ulcers and gastric cancer (22, 23). sion of its components at the appropriate time and within the Motility is essential for these bacteria to invade cultured cells, May/June 2014 Volume 5 Issue 3 e01349-14 ® mbio.asm.org 1 Downloaded from Gao et al. colonize animals, and cause disease in susceptible hosts (24–27). discrepancies. The previous studies, which identified 195 and 233 In addition to their unique structural features revealed by cryo- potential essential genes, involved a much smaller transposon in- mbio.asm.org electron tomography (12), Campylobacter and Helicobacter fla- sertion library (~7,000 insertions) and used microarrays instead gella exhibit unique aspects in the regulation of the expression of of next-generation sequencing to determine the transposon inser- their flagellar genes and in the assembly of their flagellar structure tion sites. The use of microarrays does not allow the elimination of (28, 29). For example, C. jejuni flagellar assembly, which occurs at insertions close to the 3= end of an open reading frame, which may the poles, requires the posttranslational glycosylation of the flagel- lead to insertions resulting in a functional product. Furthermore, on August 16, 2016 - Published by lin subunits and is specifically coordinated with cell division (30– the transposon element used in our study minimized polar tran- 33). Regulation of flagellar gene expression in Campylobacter and scriptional effects, potentially allowing insertions upstream of a Helicobacter is also unique, involving a two-component system cotranscribed essential gene. This feature may help to account for (FlgRS), the FlhF GTPase, and the transcription factors sigma54 the smaller size of the list of essential genes reported here. In sum- and sigma28 (34–36). Here we have identified several novel com- mary, the transposon insertion library exhibited robust coverage ponents of the C. jejuni flagellar system through a high- of the C. jejuni genome and provided insight into C. jejuni essen- throughput screen. We present data that collectively indicate that tial genes. these novel genes encode factors that directly influence motility. Identification of C. jejuni motility genes by searching for The newly identified components are highly conserved in but mutants unable to invade cultured mammalian cells. Key struc- largely restricted to Epsilonproteobacteria. This report significantly tural features of the flagellar apparatus in Epsilonproteobacteria enhances our understanding of the unique flagellar system of diverge from those of model organisms such as E. coli and S. Ty- mbio.asm.org these bacterial taxa and highlights the versatility of this nanoma- phimurium (12). These differences are more than likely attribut- chine with respect to its ability to adapt its design to the specific able to unidentified flagellar components specific to Epsilonpro- needs of diverse bacteria. teobacteria. These components cannot be identified with strategies that rely on amino acid sequence homology to known flagellar RESULTS proteins (43, 44). Consequently, we set out to carry out a genetic Construction and characterization of a C. jejuni transposon screen to identify flagellar components unique to Campylobacter mutant library by INSeq: insights into essential genes. Trans- and other Epsilonproteobacteria. Previous genetic screens for C. je- poson mutagenesis coupled to next-generation sequencing is a juni nonmotile mutants have relied on assays that are not amena- powerful tool to carry out high-throughput mutant screens in ble to high throughput and therefore have not been comprehen- bacteria (37–39). We established a genome-wide disruption li- sive (40, 45, 46). Here, we carried out a high-throughput genetic brary in C. jejuni 81-176 with a sequencing-adapted mariner screen that comprehensively searched the virulent strain of C. je- transposon
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