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The tsetse flies� intestinal microflora: a review


Anne Geiger1,*, Marie-Laure Fardeau2, Flobert Njiokou3, Bernard Ollivier2


1UMR 177, IRD-CIRAD, CIRAD TA A-17/G, Campus International de Baillarguet, 34398 Montpellier Cedex 5, France
2Aix-Marseille University, Mediterranean Institute of Oceanography (MIO), UMR/ IRD 235, UMR/CNRS 7294 Equipe MEB, ESIL, Case 925, Marseille, France
3Faculty of Science, University of Yaound� I, BP 812, Yaound�, Cameroon



*Corresponding Author: Dr. Anne Geiger
Address: UMR 177, IRD-CIRAD, CIRAD TA A-17/G, Campus International de Baillarguet, 34398 Montpellier Cedex 5, France.
Phone: +33 (0)4 67 59 39 25
Fax: +33 (0)4 67 59 38 94
E-mail: anne.geiger@ird.fr









Abstract
Human African Trypanosomiasis is caused by trypanosomes transmitted to humans by the tsetse fly, in which they accomplish their development into their infective metacyclic form. 
Large communities of microorganisms were shown to be insect inhabitants. The crucial step in the trypanosome survival occurs when it invades the fly midgut. Bacteria species were shown to play a key role in the development of pathogens in several insects. This mini-review aims to overview the present knowledge on the gut-associated bacteria in tsetse flies and their possible effects on tsetse flies infection. 



























Keywords: Human African Trypanosomiasis, bacteriome, trypanosome, tsetse flies, interactions
Insects are hosts for a large panel of microorganisms that have developed a variety of interactions ranging from mutualistic to parasitic (Jeyaprakash et al., 2003; Schmitt-Wagner et al., 2003; Campbell et al., 2004; Hongoh et al., 2005). The exact nature of many of these interactions remains poorly understood and poorly documented. Human African trypanosomiasis (HAT) is caused by protozoan parasites belonging to the species Trypanosoma brucei sensu lato. It is one of the neglected tropical diseases, a group of chronic disabling infections affecting more than 1 billion people worldwide but mainly in Africa and mostly in rural areas, poor urban environments, or in conflict zones. Two of the T. brucei subspecies, T. brucei gambiense and T. b. rhodesiense, are responsible, respectively, for the chronic form of HAT in Western and Central Africa, and the acute form of the disease in East Africa, respectively. The third subspecies, T. b. brucei is not implicated in human infection but causes animal trypanosomiasis, called Nagana, which causes dramatic economic losses to African agriculture (Reinhardt, 2002).
A possible strategy to control the disease could consist in controlling the capacity of the vector, the tsetse fly, to acquire the trypanosome which completes its biological cycle and multiplies in the fly, and/or in controlling other steps involved in its transmission to the human or animal hosts. The fly intestinal bacterial flora, most probably interacts, positively or negatively, with the parasite that shares the same habitat at the first step of fly infection. Thus, the importance to identify the host gut microflora; the underlying idea is that some of these bacteria could become a tool to combat the trypanosome within its vector, and thus, to control fly vector competence.
Tsetse fly is known to harbour three symbionts the role of which is abundantly documented. Recent works reported that many bacteria, other than symbionts are also fly�s gut inhabitants. The aim of this paper is to synthetize the current knowledge on the fly gut bacteria, their diversity and their known or possible effect on their host. 
The tsetse fly symbionts
The tsetse fly harbors three symbiotic microorganisms (Aksoy, 2000): (i) the obligate primary symbiont, Wigglesworthia glossinidia (Aksoy, 2000; Akman et al., 2002); (ii) Wolbachia (O�Neill et al.,1993), belonging to the Rickettsiaceae family, which infects a broad range of insect species, causing a variety of reproductive abnormalities, and cytoplasmic incompatibility in tsetse flies (Alam et al., 2011); and (iii) the secondary symbiont Sodalis glossinidius, belonging to the Enterobacteriaceae family (Dale and Maudlin, 1999). 
Wigglesworthia spp. maintains an obligate mutualism with tsetse; this symbiont and its tsetse fly host are believed to have co-evoluted since 50-80 million years (Chen et al., 1999). It is localized intracellularly in specialized host cells (bacteriocytes) at the anterior midgut. An additional extracellular Wigglesworthia population is hosted in the female milk glands, allowing maternal vertical transmission of the symbiont to the fly�s progeny (Ma and Denlinger, 1974; Balmand et al., 2013). The symbiont fulfils several crucial roles, both in providing its host with B-vitamins that lacks in the tsetse blood diet (Nogge, 1981; Akman et al., 2002; Rio et al., 2012; Snyder et al., 2012), and in contributing to the maturation of the host immunity (Weiss et al., 2011; Wang et al., 2009; Weiss et al., 2012). Flies lacking the Wigglesworthia bacteriome populations are sterile (Nogge, 1976; Pais et al., 2008; Alam et al., 2011). Their fecundity can however be partially restored when supplementing the blood meal with B-vitamins or yeast extract (Nogge, 1981; Alam et al., 2011). The presence of the symbiont in the tsetse�s larva also contributes to the proper development, when becoming an adult fly, of the peritrophic matrix separating the epithelial cells from the contents of the lumen, which regulates the timing of immune induction following parasite challenging with trypanosomes (Weiss et al., 2013). Wigglesworthia also impacts tsetse digestion, temperature sensitivity and susceptibility to infection with trypanosomes (Wang et al., 2009; Pais et al., 2008; Weiss et al., 2013). Weiss et al. (2011, 2012) also reported Wigglesworthia to be involved in fly protection to Escherichia coli infection; it also may promote the development of the tsetse immune system. Furthermore, it was shown that interactions between Wigglesworthia and the tsetse peptidoglycan recognition protein (PGRP-LB) may be involved in trypanosome transmission (Wang et al., 2009). 
The �-Proteobacterium, Wolbachia, is a parasitic symbiont infecting many different invertebrates including the tsetse fly (O'Neill et al., 1993; Hilgenboecker et al., 2008; Werren et al., 2008). Its habitat is restricted to the reproductive organs (Zhou et al., 1998; Cheng and Aksoy, 1999). While the prevalence of Wolbachia infections is high in laboratory-reared fly colonies (Cheng et al., 2000), field populations prevalence are much more limited, and several tsetse fly species were never shown to harbour the symbiont (Doudoumis et al., 2012). Nevertheless, the association between the some tsetse fly species and the symbiont may have a long co-evolutionary history, as Wolbachia loci were found horizontally transferred into the host genome (Doudoumis et al., 2012). Wolbachia is transovarially transmitted from one generation to the next. It has recently been reported to induce host cytoplasmic incompatibility. Furthermore, populations of female flies harbouring Wolbachia were shown to have increased fertility and increased progeny as Wolbachia negative female flies (Alam et al., 2011). 
Sodalis glossinidius is a secondary symbiont of the tsetse fly. Isolates from different tsetse species were shown to be genetically very similar indicating either the occurrence of horizontal transfer events between tsetse species, or recent independent acquisition of the bacterium by each species (Aksoy, 1995; Chen et al., 1999). Its specific elimination has been reported to result in a reduction in tsetse fly longevity (Dale and Welburn, 2001). Despite Sodalis is mainly located in the fly�s gut, it displays a large tropism for other organs such as the salivary glands, hemolymph and muscle (Cheng and Aksoy, 1999). 
Sodalis glossinidius has been shown previously to be involved in the fly's vector competence by favouring parasite installation in the insect midgut through the production of N-acetyl glucosamine (Maudlin and Ellis, 1985; Welburn and Maudlin, 1999). This sugar, resulting from chitin hydrolysis from the fly pupae by a S. glossinidius-produced endochitinase, was reported to inhibit a tsetse-midgut lectin lethal for the procyclic forms of the trypanosome (Welburn and Maudlin, 1999; Dale and Maudlin,  HYPERLINK "http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3721001/" \l "B13" 1999). The involvement of the symbiont in tsetse vector competence was confirmed by the results of a vast epidemiological campaign conducted in the Bipindi and the Campo historical sleeping sickness foci of the southern part of Cameroon. Despite very large differences between the two populations of flies regarding the prevalence of trypanosome infections and the presence of S. glossinidius in the tsetse flies, the rate of infected flies harboring S. glossinidius was very similar (75%) in both fly populations (Farikou et al., 2010). This means that, statistically, tsetse flies harboring the symbiont will have a three times greater probability of being infected by trypanosomes than those that do not harbor S. glossinidius. The results also show that the genetic structure of S. glossinidius varies at different geographical scales, with a significant differentiation between the Campo and Bipindi HAT foci (Farikou et al., 2011). Furthermore, it was shown that different fly species harboured Sodalis populations differing in their genetic structure (Geiger et al., 2005). Finally, experimental infections, demonstrated a statistic significant association between tsetse fly susceptibility to trypanosome infection and the presence of specific Sodalis genotypes (Geiger et al., 2007).

Non-symbiotic bacterial inhabitants of the fly midgut
The bacterial flora composition of the tsetse fly has only recently gained attention. Studies on tsetse flies have been conducted both on insectary-reared Glossina papalis gambiensis flies and on flies belonging to several Glossina species collected in HAT foci in Angola and Cameroon (Geiger et al., 2009, 2010, 2011), and on G. fuscipes fuscipes flies from Kenya (Lindh and Lehane, 2011). 
Regarding fly populations from Angola and Cameroon, the global fly infection rates were nearly similar (respectively 54 and 53.1%). However, they differed greatly in the diversity of the gut bacterial inhabitants. Based on morphological, nutritional, physiological, and phylogenetic criteria, the bacteria from the gut microflora from flies collected in Angola were shown to belong to the genera Enterobacter (the most frequently isolated), Enterococcus, and Acinetobacter. In Cameroon, the tsetse flies were sampled in three villages of the Campo HAT focus. The bacteria diversity was much greater than in the fly population from Angola, as nine different genera were identified, the three formerly identified bacteria and six additional genera: Chryseobacterium, Sphingobacterium, Providencia, Lactococcus, Pseudomonas, and Staphylococcus. Surprisingly, representatives of the different phyla were unevenly distributed both among the three Glossina species analyzed (Glossina palpalis palpalis, G. pallicera, and G. nigrofusca), and between the three villages even though they belonged to the same HAT focus. 
In Kenya, Lindh and Lehane (2011) investigated on the gut microflora of populations of Glossina fuscipes fuscipes. Global fly infection prevalence reached 72%, and 23 different bacterial species were identified. Sixteen species belong to the Firmicutes phylum of which seven belonged to the genus Bacillus. The other two representing phyla were Proteobacteria and Actinobacteria including an Arthrobacter sp. Among the Gamma-proteobacteria, four species belonged to the Enterobacteriaceae family. Finally two bacterial species, Bacillus subtilis and Serratia marcescens, were identified with the DNA based method (Lindh and Lehane, 2011), in contrast to the former that were identified in culture-dependent methods. 
Similar investigation was performed on insectary-reared Glossina palpalis gambiensis flies; it resulted in the identification and the characterization of a novel bacteria species, Serratia glossinae (Geiger et al., 2010). None other bacteria species was identified in those tsetse flies, and, by now, S. glossinae was never isolated from field collected flies.
 Tsetse flies are monophagous, they only feed on vertebrate blood throughout their life span, thus the high prevalence and diversity of the bacteria inhabiting the gut was unexpected. May the flies ingest bacteria present in the environment, particularly on the skin of the animals on which they feed? This could explain the gut microbiota diversity as tsetse flies feed on a variety of hosts (Simo et al., 2008; Farikou et al., 2010), which may carry diverse bacteria on their hair and skin. 

Several mechanisms may be involved in the modulation of parasite infection by midgut microbiota. One could be the competition for limited resources or the production of antiparasitic molecules by the bacteria inhabiting the vectors� gut. S. marcescens and Pseudomonas aeruginosa (Maeda and Morihara, 1995) produced cytotoxic metalloproteases. Enterobacter spp., E. coli, S. marcescens, and Enterococcus spp. (Hertle et al., 1999; Coburn and Gilmore, 2003) produced hemolysins. These molecules could impair parasite development. Antibiotics can be produced by Serratia spp. (Thomson et al., 2000); hemagglutinins (Gilboa-Garber, 1972) and siderophore by P. aeruginosa (Schalk et al., 2002). An antitrypanosomal factor has been shown to be produced by P. fluorescens (Mercado and Colon-Whitt, 1982). Prodigiosin are produced by the Gram-negative bacteria such as Serratia spp. and Enterobacter spp. (Moss, 2002). Prodigiosin was shown to be toxic for P. falciparum (Lazaro et al., 2002) and T. cruzi (Azambuja et al., 2004). Dong et al. (2009) suggested the bacteria-mediated anti-plasmodium effect was due to the mosquito�s antimicrobial immune responses. Recently, in Zambia, Enterobacter spp. were isolated from wild mosquitoes resistant to infection with P. falciparum. It was suggested the anti-Plasmodium effect was caused by bacterial generation of reactive oxygen species (Cirimotich et al., 2011).
To conclude, the review points out on the very high number of findings that have been obtained since at least two decades on the tsetse fly symbionts, and more recently on the other bacteria of the gut micro flora. It also highlights the crucial need of further investigations first in order to get a more complete insight in the actual microflora diversity with reference to the Glossina species and the diversity of the geographic location of the HAT foci. A second field of research should consist in identifying, among these bacteria, some that could modulate the fly�s vector competence, as do the endosymbionts, at least Sodalis glossinidius. Non symbiotic bacteria would in fact be easier to manipulate or to select as to optimize, for instance, the production of anti trypanosomal components. In turn such approach should also need researches on the biological interactions between the fly and the bacteria, especially the transmission of the latter to the fly�s progeny. Such investigations deserves to be undertaken  as, in case of success, they will provide novel tools to act upon the tsetse vector competence and, consequently, to fight the sleeping sickness.












Acknowledgments
This study has been supported by the Institut de Recherche pour le D�veloppement (IRD).

Conflict of interest statement
There is no conflict of interest with respect to funding or any other issue.

















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