Tsetse-Wolbachia symbiosis: Comes of age and has great potential for pest and disease control

Doudoumis, Vangelis; Alam, Uzma; Aksoy, Emre; Abd-Alla, Adly M. M.; Tsiamis, George; Brelsfoard, Corey L.; Aksoy, Serap; Bourtzis, Kostas

doi:10.1016/j.jip.2012.05.010

Cited by 55 publications

(50 citation statements)

References 149 publications

(205 reference statements)

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“…A simple check showed that a majority of the 725 "Ca. Arsenophonus" protein-coding genes returned the best or second-best BLAST hits corresponding to the genus Arsenophonus (664) or the closely related genera Providencia, Proteus, Photorhabdus, and Xenorhabdus (16). Eighteen hypothetical proteins did not return any hit; for 27 of the remaining genes phylogenetic affinity is less clear and will require more detailed phylogenetic analysis.…”

Section: Figmentioning

confidence: 99%

“…Both symbionts are vertically transmitted via milk glands (7,9,10) and are presumed to compensate for the nutritionally unbalanced blood diet (11)(12)(13)(14)(15). This highly specific microbiome of tsetse flies is usually accompanied by reproductive manipulators from the genus Wolbachia (16) and a diversity of other transient bacteria of unknown relationship to the host (17,18). In contrast to Glossinidae, the family Hippoboscidae is a species-rich, highly diversified, and cosmopolitan group feeding on mammals and birds (4).…”

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confidence: 99%

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Arsenophonus and Sodalis Symbionts in Louse Flies: an Analogy to the Wigglesworthia and Sodalis System in Tsetse Flies

Nováková

Husník

Šochová

et al. 2015

Appl Environ Microbiol

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bSymbiosis between insects and bacteria result in a variety of arrangements, genomic modifications, and metabolic interconnections. Here, we present genomic, phylogenetic, and morphological characteristics of a symbiotic system associated with Melophagus ovinus, a member of the blood-feeding family Hippoboscidae. The system comprises four unrelated bacteria representing different stages in symbiosis evolution, from typical obligate mutualists inhabiting bacteriomes to freely associated commensals and parasites. Interestingly, the whole system provides a remarkable analogy to the association between Glossina and its symbiotic bacteria. In both, the symbiotic systems are composed of an obligate symbiont and two facultative intracellular associates, Sodalis and Wolbachia. In addition, extracellular Bartonella resides in the gut of Melophagus. However, the phylogenetic origins of the two obligate mutualist symbionts differ. In Glossina, the mutualistic Wigglesworthia appears to be a relatively isolated symbiotic lineage, whereas in Melophagus, the obligate symbiont originated within the widely distributed Arsenophonus cluster. Although phylogenetically distant, the two obligate symbionts display several remarkably similar traits (e.g., transmission via the host's "milk glands" or similar pattern of genome reduction). To obtain better insight into the biology and possible role of the M. ovinus obligate symbiont, "Candidatus Arsenophonus melophagi," we performed several comparisons of its gene content based on assignments of the Cluster of Orthologous Genes (COG). Using this criterion, we show that within a set of 44 primary and secondary symbionts, "Ca. Arsenophonus melophagi" is most similar to Wigglesworthia. On the other hand, these two bacteria also display interesting differences, such as absence of flagellar genes in Arsenophonus and their presence in Wigglesworthia. This finding implies that a flagellum is not essential for bacterial transmission via milk glands. E volution of insect-bacterium symbiosis has resulted in a variety of associations in a broad range of insect taxa. Many traits of these associations (e.g., specifics of the arrangement of the host and symbiont metabolism, location of the symbionts, etc.) have been shown to reflect the ecological type of the symbiosis (i.e., obligate mutualism versus facultative symbiosis) and the host's nutritional demands due to the insufficiency of the diet (1-3). For example, phytophagous insects feeding on plant sap (e.g., aphids, whiteflies, or psyllids) and exclusively hematophagous insects (e.g., tsetse flies, sucking lice, and bedbugs) are the two most frequently studied ecological groups harboring obligate mutualistic symbionts (1, 3). However, compared to the large amount and complexity of the data accumulated on the sap-feeding insects, our knowledge on the symbioses in hematophagous insects is still limited, despite the number of species playing a crucial role as vectors for numerous pathogens, often causing a major burden to public health and world econo...

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Section: Figmentioning

confidence: 99%

mentioning

confidence: 99%

Arsenophonus and Sodalis Symbionts in Louse Flies: an Analogy to the Wigglesworthia and Sodalis System in Tsetse Flies

Nováková

Husník

Šochová

et al. 2015

Appl Environ Microbiol

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“…One trypanosome control strategy that relies on symbiont interactions is known as paratransgenesis (for more details, see references 25, 26, and 125). Paratransgenesis involves manipulating Sodalis to express antitrypanosomal effector molecules and utilizes the cytoplasmic incompatibility properties of Wolbachia (59,126) to drive the genetically modified symbiont into natural populations.…”

Section: Understanding the Tsetse Holobiont For Enhanced Vector Controlmentioning

confidence: 99%

Interwoven Biology of the Tsetse Holobiont

Snyder

Rio

2013

J Bacteriol

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Microbial symbionts can be instrumental to the evolutionary success of their hosts. Here, we discuss medically significant tsetse flies (Diptera: Glossinidae), a group comprised of over 30 species, and their use as a valuable model system to study the evolution of the holobiont (i.e., the host and associated microbes). We first describe the tsetse microbiota, which, despite its simplicity, harbors a diverse range of associations. The maternally transmitted microbes consistently include two Gammaproteobacteria, the obligate mutualists Wigglesworthia spp. and the commensal Sodalis glossinidius, along with the parasitic Alphaproteobacteria Wolbachia. These associations differ in their establishment times, making them unique and distinct from previously characterized symbioses, where multiple microbial partners have associated with their host for a significant portion of its evolution. We then expand into discussing the functional roles and intracommunity dynamics within this holobiont, which enhances our understanding of tsetse biology to encompass the vital functions and interactions of the microbial community. Potential disturbances influencing the tsetse microbiome, including salivary gland hypertrophy virus and trypanosome infections, are highlighted. While previous studies have described evolutionary consequences of host association for symbionts, the initial steps facilitating their incorporation into a holobiont and integration of partner biology have only begun to be explored. Research on the tsetse holobiont will contribute to the understanding of how microbial metabolic integration and interdependency initially may develop within hosts, elucidating mechanisms driving adaptations leading to cooperation and coresidence within the microbial community. Lastly, increased knowledge of the tsetse holobiont may also contribute to generating novel African trypanosomiasis disease control strategies.

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“…Although the presence of Wolbachia has been reported in a limited number of tsetse flies samples (Cheng et al, 2000; O’Neill et al, 1993), a thorough investigation for the presence of this symbiont, particularly in natural populations, as well the genotyping of these infections was lacking. One of the specific objectives of this CRP was to study the prevalence, genotyping and phylogenetic analysis of Wolbachia infections in both laboratory and natural populations of Glossina species including the investigation of the potential reproductive effects this infection may have in tsetse flies (see Doudoumis et al 2013; Wang et al 2013, Schneider et al 2013; (Alam et al, 2012; Doudoumis et al, 2012). …”

Section: Current Statusmentioning

confidence: 99%

Improving Sterile Insect Technique (SIT) for tsetse flies through research on their symbionts and pathogens

Abd-Alla¹,

Bergoin²,

Parker³

et al. 2013

Journal of Invertebrate Pathology

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Tsetse flies (Diptera: Glossinidae) are the cyclical vectors of the trypanosomes, which cause human African trypanosomosis (HAT) or sleeping sickness in humans and African animal trypanosomosis (AAT) or nagana in animals. Due to the lack of effective vaccines and inexpensive drugs for HAT, and the development of resistance of the trypanosomes against the available trypanocidal drugs, vector control remains the most efficient strategy for sustainable management of these diseases. Among the control methods used for tsetse flies, Sterile Insect Technique (SIT), in the frame of area-wide integrated pest management (AW-IPM), represents an effective tactic to suppress and/or eradicate tsetse flies. One constraint in implementing SIT is the mass production of target species. Tsetse flies harbor obligate bacterial symbionts and salivary gland hypertrophy virus which modulate the fecundity of the infected flies. In support of the future expansion of the SIT for tsetse fly control, the Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture implemented a six year Coordinated Research Project (CRP) entitled “Improving SIT for Tsetse Flies through Research on their Symbionts and Pathogens”. The consortium focused on the prevalence and the interaction between the bacterial symbionts and the virus, the development of strategies to manage virus infections in tsetse colonies, the use of entomopathogenic fungi to control tsetse flies in combination with SIT, and the development of symbiont-based strategies to control tsetse flies and trypanosomosis. The results of the CRP and the solutions envisaged to alleviate the constraints of the mass rearing of tsetse flies for SIT are presented in this special issue.

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Tsetse-Wolbachia symbiosis: Comes of age and has great potential for pest and disease control

Cited by 55 publications

References 149 publications

Arsenophonus and Sodalis Symbionts in Louse Flies: an Analogy to the Wigglesworthia and Sodalis System in Tsetse Flies

Arsenophonus and Sodalis Symbionts in Louse Flies: an Analogy to the Wigglesworthia and Sodalis System in Tsetse Flies

Interwoven Biology of the Tsetse Holobiont

Improving Sterile Insect Technique (SIT) for tsetse flies through research on their symbionts and pathogens

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