Campylobacter Ecology and Evolution | Book
Caister Academic Press
Samuel K. Sheppard
Medical Microbiology and Infectious Diseases, Swansea University, Swansea, UK
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Members of the genus Campylobacter are commonly found in the gastrointestinal tract of mammals and birds, and can be commensal or pathogenic in nature. For example, Campylobacter jejuni can be a harmless commensal organism in poultry and other avian and animal hosts but in humans, it is pathogenic and the most common cause of bacterial gastroenteritis worldwide. In recent years, the application of DNA sequencing and 'omics' technologies to large numbers of isolates has allowed Campylobacter research to advance rapidly revealing fascinating new insights into the cellular biology and evolution of this highly variable group of bacteria.
In this book, internationally recognised experts critically review and provide novel insights into important aspects Campylobacter research. The book is divided into four sections: Mechanisms of evolution; Adaptations to host colonisation; Molecular epidemiology; and Ecology in poultry. The topics covered range from the mechanisms of evolution through the processes of host colonisation and within host adaptation, and epidemiology to considerations of their broader biochemical and ecological properties. An important resource summarising our current knowledge of Campylobacter ecology and evolution, this book is essential reading for all researchers working with Campylobacter and related organisms.
Table of contents
1. A Candidate Hopeful Monster in the Genus Campylobacter
Samuel K. Sheppard and Daniel Falush
Analysis of genetic variation in Campylobacter - through identification of mosaic alleles, mixed species multilocus sequence types and genome wide introgression - has shown evidence for progressive hybridization of the species C. jejuni and C. coli. The resultant hybrid C. coli lineages have proliferated in agricultural animals and have emerged as the major cause of C. coli infection in humans. It is entirely unexpected that bacteria with such high sequence divergence, as far from each other at the nucleotide level as marmoset and human, could exchange almost a quarter of their genome and this finding challenges common assumptions within evolutionary biology and influential theories about how gene networks evolve. Here we discuss the possibility that agricultural C. coli originated as a hopeful monster and consider this natural setting as a model system within which the fitness effects of introgression can be investigated in unprecedented detail.
2. Learning About Recombination in Campylobacter
Paul Fearnhead, Patrick J. Biggs and Nigel French
How important a role does recombination play in the evolution of Campylobacter? In this chapter we overview some of the methods people have used to answer this question. The focus is on the importance of recombination relative to mutation in terms of generating genetic diversity within C. jejuni. We see that recombination events appear to occur at a similar rate to mutation, but can potentially have a much greater effect in terms of the changes it makes on the DNA sequence. Looking forward, the increasing availability of full- genome data has the potential to transform our detailed knowledge about the recombination process, and its role in the evolution, of Campylobacter.
3. Within-host Evolution of Campylobacter jejuni
John P. Jerome and Linda S. Mansfield
Pathogens can adapt to the host environment through changes in gene expression or by selection for mutations. For bacterial pathogens within-host gene expression has been studied extensively, but adaptation through mutation during infection has only been lightly researched. However, by comparing ancestral and host-passaged populations, researchers have shown that C. jejuni is able to rapidly adapt during infection by heritable changes. Host passage of C. jejuni often leads to increased flagellar motility - an important phenotype that enhances C. jejuni-host interactions. In addition, host passage results in C. jejuni with increased rates of colonization, and with higher virulence, during subsequent host infections. Recently, homopolymeric DNA tract mutations, and large-scale genomic rearrangements, have been implicated as potential mechanisms for these phenotypic changes. In the future, advances in sequencing technologies and predictive models of homopolymeric DNA mutability will help to elucidate the mechanisms underlying the ability of C. jejuni to rapidly adapt by genetic change during host infection.
4. Concerted Evolution in Campylobacter jejuni and Campylobacter coli
Richard J. Meinersmann
Concerted evolution is the phenomenon in which multiple copies of genes maintain sequence similarity in a single individual while the genes continue to diverge between individuals. Concerted evolution has been described in Campylobacter jejuni and C. coli for the pair of flagellin genes, which are notable for their diversity, the 23S ribosomal RNA genes, which are notable for the degree that they are conserved, and for the portion of the ribosomal operon between the 16S and 23S genes. The evidence for concerted evolution is presented and the biological implications are discussed in this review. An interesting case is the concerted evolution of the 23S rRNA genes that is needed to rapidly become resistant to macrolides. Understanding which genes are affected by concerted evolution will allow proper assessment of probable phylogenetic distortions that will be seen with such genes.
5. Genome and Transcriptome Evolution in the Genus Campylobacter
My Thanh Le and Arnoud H.M. van Vliet
The genus Campylobacter belongs to the Epsilon-subdivision of the Proteobacteria, and comprises a large number of species, which includes the important human pathogen Campylobacter jejuni. The recent progress in high-throughput sequencing technologies are leading to a rapid increase in information on C. jejuni and other Campylobacter species, and these data are beginning to feed into studies on transmission, infection and evolution of this highly variable group of bacteria. The genomes of Campylobacter species display significant levels of variation at the level of genes, promoters, operons, and gene order. This may be explained by the relative paucity of DNA repair mechanisms and horizontal gene transfer via natural transformation, phase variation, plasmid transfer and infection with bacteriophages. In this chapter we will review the current state of genomics and transcriptomics of Campylobacter species, and highlight opportunities where further progress may be made in our understanding of the evolution of Campylobacter.
6. Repetitive DNA: A Major Source of Genetic Diversity in Campylobacter Populations?
Jack Aidley and Christopher D. Bayliss
A marked feature of the genomes of Campylobacter jejuni and other Campylobacter species is the presence of long polyG tracts within the reading frames of genes. Instability in these repetitive DNA sequences leads to frequent, reversible switches in expression of the associated genes termed phase variation. High rates of phase variation have been detected for C. jejuni genes using reporter constructs and antibodies and these high switching rates enable rapid access to hundreds of different phenotypes. Observations of C. jejuni populations from in vitro and in vivo populations indicate the presence of many of these phase variable phenotypes. We speculate on the forces driving the distributions of these phase variable genotypes and on the potential impact of phase variation on the commensal and disease-causing attributes of C. jejuni.
7. Campylobacter Strategies for Colonizing the Host Gastrointestinal Tract
Annika Flint, James Butcher and Alain Stintzi
Colonizing the gastrointestinal tract is fraught with multiple challenges for incoming bacteria. These microbes must not only evade the host immune systems and the harsh environmental conditions of the gastrointestinal tract, but also out-compete the native microbiota. Campylobacter jejuni is an efficient colonizer of both avian and mammalian hosts. In both these environments, C. jejuni is able to scavenge and metabolize the nutrients found within the mucus layer and out-compete commensal microbes. To accomplish this feat, C. jejuni preferentially metabolizes specific constituents within the mucus layer of the intestine as growth substrates, including key amino acids and fucose. This chapter provides an overview of the pathways and mechanisms of C. jejuni important for adaptation, survival and growth within the gastrointestinal tract.
8. The Intricate Relationship Between Campylobacter and Mucus
Claire Shortt, Gina Duggan and Billy Bourke
For any successful mucosal pathogen a key early step in the infection sequence is to establish effective colonisation of the mucus layer. Campylobacters have evolved to live as commensals in the mucus of avian species. In disease in humans these organisms can breach the mucus defence systems and interact directly with intestinal epithelial cells. Recent insights into the role of mucus in protecting the intestine and the influence of mucus on the behaviour and adaptaion of C. jejuni, has led to a much better understanding of the ecology of C. jejuni in the supra mucosal niche.
9. Campylobacter Association with the Human Host
Abiyad Baig and Georgina Manning
Campylobacter jejuni is a foodborne pathogen and the major cause of gastroenteritis in humans worldwide. Adhesion to, and invasion of, host epithelial cells have been investigated as important mechanisms in the infection process. Many genes have been identified that are proposed to be involved in the interaction with host cells and many mechanisms suggested. C. jejuni seems to be an opportunistic pathogen in humans so an important question is: are there any real 'virulence factors' or are there several different mechanisms utilised by different strains of this organism to access the human niche? Furthermore, many studies have focussed on a single strain, however it is known that invasion potential varies among C. jejuni strains and human clinical isolates are generally more invasive compared to non-clinical isolates. There may be much to be learned from studying phenotypically-related strains. This chapter will review the current understanding of the mechanisms of host cell interaction and will explore whether the use of a phenotypically-related group of hyper-invasive strains can shed any light as to how C. jejuni has evolved to become an invasive pathogen.
10. Siderophore-mediated Iron Acquisition for Campylobacter Infection
Ximin Zeng and Jun Lin
Iron acquisition is critical for bacterial pathophysiology. The high-affinity iron acquisition mediated by siderophores is the most efficient and common iron scavenging mechanism in Gram-negative bacteria. While Campylobacter does not produce any siderophores, siderophore piracy is evident in various Campylobacter species. To date, enterobactin, a triscatecholate siderophore with the highest affinity for ferric iron, is the only known physiologically relevant siderophore utilized by Campylobacter for in vivo colonization. Recent studies have revealed novel features of ferric enterobactin acquisition systems in Campylobacter, provided new insights into the evolution of ferric enterobactin acquisition in different Campylobacter species, and suggested that Campylobacter is an ideal model organism to examine key issues of enterobactin-mediated iron scavenging. Salmochelin, the glucosylated enterobactin, is likely another significant iron source for Campylobacter during infection. This chapter also discusses the ecology of potential siderophores and corresponding producers as an iron source in the intestine and discusses the role of siderophore-mediated iron scavenging in the pathogenesis of Campylobacter and other enteric pathogens.
11. Genetic Mechanisms Involved in Campylobacter jejuni Survival Under Oxidative Stress Conditions
Ozan Gundogdu, Brendan W. Wren and Nick Dorrell
Campylobacter jejuni is the major cause of human bacterial gastroenteritis. As a microaerophilic bacterium, C. jejuni will be exposed to reactive oxygen species (ROS) during the course of normal bacterial metabolism as well as during colonisation or infection, from the host immune system. C. jejuni contains a number of different mechanisms for countering the effects of oxidative stress and the control of the C. jejuni oxidative stress response is complex involving multiple inter-linked levels of regulation, with two new regulators of the oxidative stress response recently identified. In this chapter, we cover both the mechanisms of C. jejuni oxidative stress defence and the current understanding of the increasingly complex regulation of this oxidative stress response.
12. Oxidative Stress Survival During Campylobacter Transmission and Infection
Rebecca Handley, Mark Reuter and Arnoud van Vliet
Illness from Campylobacter jejuni infection is a widespread burden in the developed world. The spread and high incidence of this pathogen is in no small part due to its ability to survive exposure to exogenous stresses. This provides C. jejuni with the opportunity to spread to and colonise a variety of niches that lack the conditions in which C. jejuni can grow. In this chapter we will describe the common transmission routes of C. jejuni, followed by a discussion of the systems and mechanisms that are part of the protective responses C. jejuni has at its disposal. Finally, we will discuss the challenges faced by C. jejuni as a microaerophilic organism, which has to survive in an aerobic world.
13. The Role of the Flagellum in Campylobacter jejuni Colonization and Disease
Jason L. O'Loughlin and Michael E. Konkel
Campylobacter jejuni causes acute human enterocolitis via mechanisms requiring colonization of the host intestine, adherence to, and subsequent invasion of epithelial cells. The C. jejuni flagellum is responsible for the motility necessary for colonization and contributes to adherence and internalization by host cells. The flagellum also secretes non-flagellar (i.e., effector) proteins that enhance internalization by modifying host cell behavior. Additionally, the flagellum is the only type three secretion system (T3SS) encoded by C. jejuni and its structure is similar to the injectisome of a classical virulence-associated T3SS common to other enteric pathogens. Numerous proteins secreted by the flagellum have been identified and characterized, with several proteins delivered to the cytosol of host cells. Furthermore, the flagellum of C. jejuni contributes to biofilm formation. Taken together, flagellar function, including the secretion of effector proteins and the characterization of their effects on the host, is an important area of C. jejuni research.
14. Does Biofilm Formation Aid Colonisation and Infection in Campylobacter?
Ben Pascoe, Hilary Lappin-Scott, Samuel K. Sheppard and Hiroshi Asakura
Biofilm formation can promote the colonisation of host and non-host environments for some bacteria. In some species cell aggregation and attachment are key pathogenic determinants. However, in Campylobacter, many questions remain about the importance of biofilms for surface attachment in order to establish an infection in animals or humans. In this chapter, we explore the factors that influence biofilm formation in Campylobacter, and discuss this in the context of invasion, colonisation and the onset of disease.
15. Alternative Infection Models for Campylobacter jejuni
Nicola J. Senior, Sok Kiang Lau, Roberto M. La Ragione and Olivia L. Champion
Research using experimental hosts enables the lifecycle, metabolism and virulence mechanisms of Campylobacter jejuni to be interpreted in a contextual manner. However, the ability of C. jejuni to cause disease appears to be dependent not only on the bacterial strain but also on the host; C. jejuni is able to cause disease in certain hosts yet it remains avirulent in other host species. Mammalian models of infection are the most widely used and best characterised models of human disease, yet there are ethical, social and scientific limitations of these models. These concerns have driven work to reduce, refine and replace mammalian models of infection and this chapter considers the use of alternative infection models for C. jejuni research. This chapter ends with a review of the metabolism of C. jejuni in the context of host adaptation.
16. Exploring the Population Dynamics of Multiple Campylobacter Strains in Poultry
Fran M. Colles and Martin C.J. Maiden
In order to reduce the burden of human Campylobacteriosis, there is an urgent need to better understand the natural ecology of Campylobacter amongst poultry flocks, so that effective on-farm intervention strategies may be designed. Broiler flocks contaminated early in the production cycle, as well as older birds, may be colonised by multiple strains of Campylobacter. There is evidence that Campylobacter strains are unevenly distributed amongst individual birds within a flock and that faecal samples are efficient in capturing diversity at a flock level. Campylobacter strains are not necessarily cleared from a flock and may persist for some time, meaning that the diversity of Campylobacter strains that can be isolated from a flock may increase over time. Groups of wild birds are typically colonised by a high diversity of Campylobacter strains which may be a consequence of diversifying selection generated by host-pathogen interactions. However, studies of Campylobacter population dynamics over more than a few weeks are hindered by conventional sampling methods and the short life cycle of broiler chicken flocks. The precise mechanisms controlling the dynamics of Campylobacter colonisation are likely to be multifactorial and remain to be fully understood.
17. Evolution of Campylobacter Species in New Zealand
Nigel French, Shoukai Yu, Patrick Biggs, Barbara Holland, Paul Fearnhead, Barbara Binney, Andrew Fox, Dai Grove-White, Jessica W. Leigh, William Miller, Petra Muellner and Philip Carter
New Zealand is an isolated archipelago in the South-West Pacific with a unique fauna and flora, a feature partly attributable to it being the last sizable land mass to be colonised by man. In this chapter we test the hypothesis that different periods in the history of New Zealand, from pre-history to post-Polynesian/pre-European arrival and post-European, have left a signature on the evolution of Campylobacter spp. that is detectable in the extant population today. In order to explore and test this hypothesis we describe a brief, relevant history of New Zealand, followed by three studies: 1) an examination of recently discovered populations of new Campylobacter spp. in endemic wild birds and environmental water; 2) a comparison of isolates from humans, ruminants and poultry in the United Kingdom and New Zealand and; 3) an examination of the phylogeny of samples of multilocus sequence typing (MLST) genotype ST-474, the strain responsible for a multi-year poultry-associated epidemic in New Zealand.
18. How Molecular Typing has Changed our Understanding on Sources and Transmission Routes of Campylobacteriosis in Finland
Caroline P. A. de Haan, Rauni I Kivistö, Hilpi Rautelin and Marja-Liisa Hänninen
In this chapter we will present a short review on data concerning the analysis of sources/reservoirs important in the epidemiology of campylobacteriosis among Finnish patients who acquired their infection from domestic sources between 1996 and 2006. We describe epidemiological studies on sporadic cases to find important risk factors and studies on water- and milk-borne outbreaks. In addition, we describe strain characterization, which includes Penner serotyping, pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). Also, we discuss results of source attribution modeling studies. Our results have shown that the strains circulating in Finland in different hosts are diverse but certain types predominate and some are present persistently in fluctuating proportions. In addition, the chicken flocks were less likely to be positive for Campylobacter compared to most other similar studies. This suggests that they may contribute less to the relative burden of human campylobacteriosis compared to estimates in some other European countries. Therefore, other sources, such as water or environmental exposure, may be additional transmission routes in Finland.
19. Extensive Spatial and Temporal Clustering of Campylobacter Infections Evident in High-Resolution Genotypes
Norval J.C. Strachan and Ken Forbes
Outbreaks of campylobacteriosis are rare with approximately 99 % of cases being individual sporadic human infection, where they are typically unrelated in time and space and presumed to be acquired from different sources. However, the sporadic nature of campylobacteriosis has yet to be evaluated at the strain level using high resolution genotyping. In this chapter we investigated most cases reported in Scotland between July 2005 and September 2006 (N=5167), where human isolates were typed by sequencing 7 multi-locus sequence typing loci and the flaA locus. Here, general and household outbreaks that were defined using epidemiological data were compared with apparently sporadic cases, with the aim of identifying clusters of cases in time and space by recognising common strain types that may indicate a common source of infection. Spatial clusters representing 5% of cases occurred in 20 of 247 ST-flaA strains, and temporal clusters representing 12-13% of cases occurred in 67 of 316 ST-flaA strains. Similar to sporadic cases, strains from both temporal and spatial clusters (mainly C. jejuni) were attributed mainly to farm ruminants and chicken. Campylobacter infections defined as genotypic strains showed up to five times more in clustered cases than was evident from recognised outbreaks using epidemiological data (general (N=3 No of cases/%) and household (N=50 No of cases/%)). These clusters of homogenous genotypes potentially reflect shared origins either via food or the environment. Analysis of isolates characterised by high-resolution genotyping revealed unexpectedly frequent cases in spatial and especially temporal clusters, suggesting that related cases often go unrecognised but are perhaps more common than initially thought.
20. Ecology and Host Associations of Campylobacter in Wild Birds
Jonas Waldenström and Petra Griekspoor
The following review aims to summarize the present knowledge on Campylobacter jejuni and other Campylobacter-species in wild birds. The question of whether campylobacters present in wildlife, especially those found in wild birds, play a role in the epidemiology of human campylobacteriosis has been around for more than 30 years (Kapperud and Rosef, 1983; Smibert, 1969). This review will summarize what is currently known and point to the gaps in understanding of these organisms and their interplay with hosts and the environment. Here the focus will mainly be on C. jejuni, as this species has received most attention, but data for Campylobacter coli and Campylobacter lari will also be discussed.
21. Epidemiology and Control of Campylobacter in Modern Broiler Production
Ana B. Vidal, Rob H. Davies, John D. Rodgers, Anne Ridley and Felicity Clifton-Hadley
Recent studies continue to indicate that poultry products remain a significant source of foodborne zoonotic Campylobacter infections. These organisms have evolved to readily colonise the avian gut and have adapted to achieve high intestinal and faecal concentrations in broiler flocks. The control of Campylobacter originating from broiler meat is the most important element of public health strategies aiming at reducing the number of human campylobacteriosis cases. This chapter describes factors related to poultry farm and abattoir environments and processing management practices that are associated with Campylobacter contamination at various levels of the broiler production chain, as well as the main available control options. Despite the large body of research in the last 20 years, including the use of molecular typing tools, the ecology and epidemiology of Campylobacter in poultry remains poorly understood, possibly as a result of ineffective detection of the organism in key environmental niches. A better understanding of the multiple interactions between this organism, the poultry environment and the chicken host is required in order to help design targeted and cost-effective control strategies in poultry production.
22. Conditional Commensalism of Campylobacter in Chickens
Lisa K. Williams, Emma K. Trantham and Tristan A. Cogan
Two species of Campylobacter, C. jejuni and C. coli, dominate the epidemiology of human infection. Both species are characterised by their broad host range, and spectrum of effects that they have on the hosts that they colonise. In non-immune humans, both cause severe gastrointestinal symptoms, as they can do in companion animals. Farmed animals, and in particular poultry, appear to carry these organisms as intestinal commensals. Given the severe disease seen in some host species this may be because the bacterium is adapted to different hosts. For example, poultry adapted strains may cause severe disease in humans which are an accidental host. Alternatively, the apparent commensalism of Campylobacter in poultry may in fact be controlled parasitism, with the host able to control, but not prevent, colonisation by the bacterium. Here we review the evidence for commensalism of Campylobacter in poultry and ask the questions: are C. jejuni and C. coli really avian commensals, or are they just well controlled pathogens?
23. The Chicken Reservoir and Specific Alleles at Conserved Contingency Loci Can Promote Host Colonization and Disease by Campylobacter jejuni
John E. Linz
Campylobacter jejuni ranks among the top foodborne bacterial pathogens in terms of number of disease cases and economic impact. Despite its clear importance as a pathogen, relatively little is known about the specific mechanisms by which C. jejuni causes disease. Twenty three or more contingency loci in C. jejuni strain 11168 are subject to high frequency mutation within homopolymeric tracts and these genetic changes impact gene expression and/or protein activity. Our laboratory is investigating the role of C. jejuni contingency loci in virulence. This chapter reviews recent work in our laboratory that demonstrates that the chicken reservoir promotes phase variation at specific contingency loci and this enhances colonization and disease in a mouse model for disease. A specific allele at contingency locus Cj0170 for example regulates C. jejuni motility and virulence in mice while specific alleles at loci Cj0045, Cj1420, and Cj0685 are strongly associated with colonization and disease. Based on our data, we hypothesize that analysis of the genotype at contingency loci provides a useful tool to predict virulence in mice and humans. The data also prompt us to focus on highly conserved contingency loci as useful targets to prevent disease in humans.
24. The Long Road Ahead: Unravelling the Immune Response to Campylobacter in the Chicken
Paul Wigley and Suzanne Humphrey
Chicken is the most important reservoir for Campylobacter, yet relatively little is known about its interaction between the chicken immune system. Campylobacter infection of the chicken gastrointestinal tract elicits an initial inflammatory response, but this differs in nature and is lower in magnitude than the well-understood response to Salmonella. Campylobacter is recognized by the host via a panel of Toll-Like Receptors (TLRs) notably TLR-4 and TLR-21. However, the response results is little pathology leading several observers to consider there is a tolerogenic response in the chicken. Campylobacter may also be invasive leading to liver infection and there is clear evidence of activation of adaptive immunity from recent transcriptional studies. The nature and role of adaptive responses is poorly understood, though maternally derived antibody is considered to protect against early colonization. This chapter reviews what is known of the immune response to Campylobacter in the chicken and the prospects of control through vaccination or breeding for genetic resistance. We will also focus on areas where future research can begin to address the considerable gaps in our knowledge.
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(EAN: 9781908230362 9781908230980 Subjects: [microbiology] [bacteriology] [medical microbiology] [molecular microbiology] )