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Trypanosoma Cruzi Immune Response Modulation Decreases Microbiota in Rhodnius Prolixus Gut and Is Crucial for Parasite Survival and Development

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Trypanosoma Cruzi Immune Response Modulation Decreases Microbiota in Rhodnius Prolixus Gut and Is Crucial for Parasite Survival and Development Trypanosoma cruzi Immune Response Modulation Decreases Microbiota in Rhodnius prolixus Gut and Is Crucial for Parasite Survival and Development Daniele P. Castro1*, Caroline S. Moraes1, Marcelo S. Gonzalez2, Norman A. Ratcliffe1, Patrı´cia Azambuja1,3, Eloi S. Garcia1,3 1 Laborato´rio de Bioquı´mica e Fisiologia de Insetos, Instituto Oswaldo Cruz, Fundac¸a˜o Oswaldo Cruz (Fiocruz), Rio de Janeiro, Rio de Janeiro, Brazil, 2 Laborato´rio de Biologia de Insetos, Departamento de Biologia Geral, Instituto de Biologia, Universidade Federal Fluminense (UFF) Nitero´i, Rio de Janeiro, Brazil, 3 Departamento de Entomologia Molecular, Instituto Nacional de Entomologia Molecular (INCT-EM), Rio de Janeiro, Rio de Janeiro, Brazil Abstract Trypanosoma cruzi in order to complete its development in the digestive tract of Rhodnius prolixus needs to overcome the immune reactions and microbiota trypanolytic activity of the gut. We demonstrate that in R. prolixus following infection with epimastigotes of Trypanosoma cruzi clone Dm28c and, in comparison with uninfected control insects, the midgut contained (i) fewer bacteria, (ii) higher parasite numbers, and (iii) reduced nitrite and nitrate production and increased phenoloxidase and antibacterial activities. In addition, in insects pre-treated with antibiotic and then infected with Dm28c, there were also reduced bacteria numbers and a higher parasite load compared with insects solely infected with parasites. Furthermore, and in contrast to insects infected with Dm28c, infection with T. cruzi Y strain resulted in a slight decreased numbers of gut bacteria but not sufficient to mediate a successful parasite infection. We conclude that infection of R. prolixus with the T. cruzi Dm28c clone modifies the host gut immune responses to decrease the microbiota population and these changes are crucial for the parasite development in the insect gut. Citation: Castro DP, Moraes CS, Gonzalez MS, Ratcliffe NA, Azambuja P, et al. (2012) Trypanosoma cruzi Immune Response Modulation Decreases Microbiota in Rhodnius prolixus Gut and Is Crucial for Parasite Survival and Development. PLoS ONE 7(5): e36591. doi:10.1371/journal.pone.0036591 Editor: Kristin Michel, Kansas State University, United States of America Received January 12, 2012; Accepted April 3, 2012; Published May 4, 2012 Copyright: ß 2012 Castro et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The work is supported by funds by Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq), Coordenac¸a˜o de Aperfeic¸oamento de Pessoa de Nı´vel Superior (CAPES), Fundac¸a˜o de Amparo a` Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Fiocruz. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction completing their developmental cycles in contrast to the Y strain which rapidly disappears from the insect’s gut [14,15]. Chagas disease is an endemic parasitic disease important in Regarding the role of the diverse gut microbiota in modulating large areas of Latin America [1]. The majority of triatomine T. cruzi development in the gut of R. prolixus, we have previously species found in this region are potential vectors for Trypanosoma identified a Serratia sp. isolated from this insect vector which cruzi, the causative agent of the disease [1,2]. Rhodnius prolixus is the interferes with some strains of parasite development and lyses main vector of Chagas disease in the northern part of South parasites in in vitro experiments [7,14,16–18]. The microbiota has America and in some areas of Central America [3]. also previously been shown to modulate the vectorial competence The T. cruzi – triatomine vector interactions are complex and of the insect host by means of direct interaction with parasites or mediated by numerous parasite and insect factors [4–8]. The by competition for resources in the gut [7–11]. In addition, parasite circulates between humans, domestic and sylvatic microbiota can constrain pathogen development indirectly by mammalian reservoirs, and insect vectors [6–8]. T. cruzi infection inducing vector antiparasitic activity and humoral immune of the insect vector starts with the ingestion of an infective blood defense factors in particular [8,12,16,19–21]. meal. A successful transmission depends upon the parasite Humoral defenses in insects are characterized by a battery of multiplication and differentiation in the triatomine gut [7–9]. potent antimicrobial peptides (AMPs), reactive intermediates of Many factors have been implicated in the establishment of T. nitrogen or oxygen, and complex enzymatic cascades, such as the cruzi infection in the insects vector gut including a crop lytic factor, prophenoloxidase system, that contribute to clotting or hemo- lectins, gut enzymes and microbiota-derived factors, antimicrobial lymph melanization [22]. These humoral factors may be secreted compounds and nitric oxide [4,6–12]. In addition, the gut directly into the hemocoel or into the gut lumen as components of structural organization is important for parasite attachment to the immune response to eliminate potential pathogens acquired the perimicrovilar membranes and their subsequent development during feeding [7,8,23]. [5,9,13]. The success of parasite infection also depends upon the In this paper, we have examined the relationship in the gut of R. T. cruzi strain used and the insects species infected. For example, in prolixus between the microbiota and the insect’s humoral R. prolixus, the T. cruzi Dm28c clone and CL strains are capable of antibacterial compounds with the level of infection following PLoS ONE | www.plosone.org 1 May 2012 | Volume 7 | Issue 5 | e36591 Trypanosoma cruzi Decreases Rhodnius Microbiota feeding with T. cruzi. In particular, we investigated the role of T. sequently infected with Dm28c clone (AC; median 0 CFU) cruzi infection in the modulation of the microbiota population in (Figure 1C; p,0.05). the R. prolixus gut. We demonstrated, for the first time, that infection with T. cruzi Dm28c clone, but not with the Y strain, Bacterial growth inhibition changes the microbiota population in the digestive tract by The anterior midgut antimicrobial activities at 9 days after modulating the host immune responses and that this contributes to feeding in the ZI assay (0.8460.04 cm diameter) were significantly parasite development in the gut of R. prolixus. higher than posterior midgut (0.0960.09 cm diameter) of control infected insects (CC) (Figure 2A; p,0.001). Therefore, the Results bacterial growth inhibition and immune reactions experiments were standardized using samples of anterior midgut. We also Trypanosoma cruzi infection and microbiota population compared with the ZI assay, the antibacterial activities of the in the digestive tract anterior midgut at days 5, 9 and 16 after infective feeding (CC), Parasite infection and microbiota population in R. prolixus 5th- and observed that at day 9 the activity (0.8460.04 cm diameter) instar nymphs whole digestive tract were analyzed from 5 to was significantly higher compared with day 5 (0.6760.02 cm 29 days after treatment. In this period, the median number of T. diameter) and day 16 (0.6460.02 cm diameter) (Figure 2B; cruzi Dm28c clone in the whole digestive tract (CC) ranged from 1 p,0.001). to 36104 parasites/ml (Figure 1A). Regarding the microbiota, the median number of gut bacteria in the control insects fed blood Gut antimicrobial activities alone (C) showed a rapid increase and by 8 days after feeding In order to obtain a better understanding of the regulation of reached a peak of 1.461011 before reducing to 86107 bacteria/ microbiota in the vector anterior midgut, the antimicrobial digestive tract by day 28 after feeding (Figure 1B) and then activities in the anterior midgut of control R. prolixus (C) and remained stable in numbers until the next feeding. Significant insects infected with T. cruzi Dm28c clone (CC) were investigated. differences in bacterial numbers between parasite-infected (CC) The results of the ZI assays showed significantly smaller zones of and control (C) groups were observed at 8 days after initiating the inhibition (ZI) in control insects (C) (0.78 cm60.03) when experiments. At this time in control insects, the microbiota compared with control infected insects (CC) (1.0 cm60.02) reached 1.461011 bacteria (CFU) whereas parasite-infected insects (Figure 3A; p,0.0001). The effect of T. cruzi Dm28c infection presented only 1.86109 CFU /digestive tract (Figures 1B, 1C; on antibacterial activities in the anterior midgut was also tested p,0.001). using a turbidometric assay (TB). Experiments incubating the To investigate the role of the reduction of the microbiota upon extracts with bacteria for 11 h at 37uC showed significantly higher T. cruzi Dm28c infection in R. prolixus, one group of 5th instar antibacterial activity in infected insects (CC) compared with nymphs was treated with antibiotic solution alone added to the control insects (C) only after 4, 5 and 6 h of incubation (Figure 3B; blood meal (A), and another group of insects was treated with p,0.05). For example, parasite-infected insects (CC), after 4 h antibiotic and then infected with parasites (AC). With this non incubation, recorded an antibacterial activity of 10.92 (60.71), toxic dose of antibiotic in the blood meal, we observed an increase significantly higher than control groups (C) with activity of 7.45 in T. cruzi Dm28c infection (AC), in comparison with insects fed (60.47) (Figure 3C; p = 0.001). These results were confirmed by with parasites alone (CC), ranging from 3.26105 parasites/ml to following bacterial growth on BHI-agar plates where control (C) 1.76105 from 8–13 days to 25–29 days, respectively, after and infected insects (CC) presented low numbers of bacteria (not shown).
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