|Year : 2018 | Volume
| Issue : 2 | Page : 69-78
Role of gut inhabitants on vectorial capacity of mosquitoes
Lekshmi Jayakrishnan1, Ambalaparambil Vasu Sudhikumar2, Embalil Mathachan Aneesh1
1 Communicable Disease Research Laboratory, Department of Zoology, St. Joseph's College, Irinjalakuda, Kerala, India
2 Department of Zoology, Christ College, Irinjalakuda, Kerala, India
|Date of Submission||11-Aug-2017|
|Date of Acceptance||14-Jun-2018|
|Date of Web Publication||1-Oct-2018|
Embalil Mathachan Aneesh
Communicable Disease Research Laboratory, Department of Zoology, St. Joseph's College, Irinjalakuda–680 121, Kerala
Source of Support: None, Conflict of Interest: None
Mosquito-borne diseases are spreading at an alarming rate. Globally millions of deaths occur due to the diseases transmitted by mosquitoes, next to AIDS and tuberculosis. Several methods have been used to control these vectors and the diseases caused by them. Earlier studies have shown the potential role of mosquito gut inhabitants on disease transmission. Their findings can be used as an innovative approach for devising strategies to modify the survival of mosquitoes by reducing their lifespan, reproduction and disease transmission abilities. In this study, microbiome of the three genera of mosquitoes, namely Aedes, Anopheles, and Culex along with their vectorial capacity have been reviewed for assessing their role in mosquito control and transmission. Relevant articles were accessed using different databases, including LILACS, Embase, Science Direct and PubMed from inception to June 2017. The search keywords included “Aedes”, “Anopheles”, “Culex”, “gut inhabitants”, “vectors”, and “mosquito”. The titles, abstract, and keywords of the retrieved articles were screened, and eligible research articles were sorted. The review indicates that paratransgenesis may be considered as a versatile and effective strategy to eradicate the spurt of mosquito transmitting diseases. Enterobacter species is the most common type of gram-negative bacteria associated with the gut of all the three genera of mosquitoes. It was found to have a beneficial effect on humans as it helps in destroying dreadful disease-transmitting vectors. These symbiotic qualities of the microbes need to be thoroughly investigated further to reveal their antipathogenic effect on the vector.
Keywords: Aedes; Anopheles; Culex; gut inhabitants; microbes; mosquito; vectorial capacity
|How to cite this article:|
Jayakrishnan L, Sudhikumar AV, Aneesh EM. Role of gut inhabitants on vectorial capacity of mosquitoes. J Vector Borne Dis 2018;55:69-78
|How to cite this URL:|
Jayakrishnan L, Sudhikumar AV, Aneesh EM. Role of gut inhabitants on vectorial capacity of mosquitoes. J Vector Borne Dis [serial online] 2018 [cited 2022 Oct 4];55:69-78. Available from: https://www.jvbd.org/text.asp?2018/55/2/69/242567
| Introduction|| |
Mosquitoes, the hexapod invertebrates belonging to the Culicidae family of Insecta class, have profound influence on human beings. More than 3555 recognized mosquito species divided into two subfamilies (Anophelinae and Culicinae) and 112 genera have been recorded in different parts of the world. India, belonging to the oriental region is regarded as one of the richest biogeographic zones for different mosquitoes. A record indicates that Indian mosquito fauna includes 393 species divided among 49 genera and 41 subgenera. Most species of this holometabolous insect remains as nonpathogenic, while some are vectors of certain dreaded diseases like malaria, chikungunya, Zika, yellow fever etc. More than one million people die every year throughout the world due to mosquito-borne diseases,,,.
The vector competences of mosquitoes are highly dependent on the microenvironment of their gut which normally undergoes radical structural remodeling during each stage of the life cycle. Hence, studies on gut content analysis of mosquito in terms of feeding (which includes diverse form of microbial flora composed of commensal or symbiotic bacteria, algae, protozoans, organic debris etc) are essential, as their feeding behaviour changes during metamorphosis from an aqueous larval stage to an aerial adult. Studying the interaction between the gut microenvironment and vector competency might be helpful in controlling vector-borne diseases without disturbing the ecological balance. Accordingly, a systematic review was made, intended to reveal the characteristic features of microbial consortia residing in the mosquito gut. For this different published research articles and reviews were assessed using the online databases, viz. LILACS, Excerpta Medica data BASE (Embase®), Science Direct and PubMed® from inception to June 2017. Other sources consulted were the CDC, WHO, and NIH websites. The search keywords included “Aedes”, “Anopheles”, “Culex”, “gut inhabitants”, “vectors”, and “mosquito”. Articles retrieved for the study were absolutely in English. The titles, abstract, and keywords of the retrieved articles were screened, and eligible research articles were sorted. The selected articles were considered reliable, if they revealed one or more perspectives about the research interest (microbial inhabitants in the gut of mosquito), irrespective of when or where the investigations or experiments were done. The study also included epidemiological and observational perspectives of gut inhabitants of Aedes, Anopheles and Culex mosquito genera, since these mosquitoes have profound effects on the public health.
Larval gut anatomy of mosquito
A prominent digestive tract appears from the larval stage of mosquitoes and it gets divided into foregut, midgut, and hindgut. In all mosquitoes, the basic structure of digestive tract is similar, however, diverse modifications have been observed in this structure due to the differences in feeding mechanisms. Presence of macro- and micro-molecular nutrients like carbohydrate and proteins, along with micronutrients in the gut provide essential resources to the microbes for multiplication,. For example, absorption of nitrogenous waste like uric acid in the hindgut provides nutritive environment for gut bacteria.
The ectodermally derived foregut and hindgut are separated from the epidermal layer by a lining of exoskeleton (made of cuticular glycoproteins and chitin); which gets shed at each ecdysis. The foregut includes pharynx (used for filtering and swallowing) and oesophagus. Hindgut is divided into an anterior portion termed as Malpighian tubules, followed by posterior fermentation chamber and rectum for holding faeces before defaecation. Endodermally derived midgut [Figure 1] a and [Figure 1]b is the primary site for digestion and absorption. Histologically, it has an epithelial outer lining consisting of a basement membrane, followed by ciliated columnar epithelial and regenerative cells, and peritrophic membrane/matrix [Figure 1]c, which is a unique feature of the midgut. In mosquitoes, this matrix bifurcate midgut into ectoperitrophic space and endoperitrophic space,,,,,. Midgut consists of cardia, gastric caeca, anterior and posterior stomach. It remains as an important passage for the blood-borne parasite since it forms a barrier between the ingested parasite and haemocoel of the host. Mosquito parasites must penetrate host gut before completing their development in host tissue to remain as pathogenic. However, the midgut remains a hostile environment for the parasite. For example, in Anopheles mosquitoes, 50% of the mosquito midgut stages of the Plasmodium berghei die naturally by apoptosis before the gut invasion. Therefore, an effective understanding of these factors can be used as a tool to control the parasitic vector microbes and check the disease transmission.
|Figure 1: (a) Larval stage of mosquito with external morphology; (b) Generalised midgut structure of mosquito larva; and (c) Epithelial lining of midgut; AMG—Anterior mid gut; PMG—Posterior mid gut.|
Click here to view
Earlier studies have reported two different types of peritrophic matrices of the midgut, one is Type I that lines the entire midgut when the food is ingested; and the other is Type II that is seen only in the anterior region of the midgut. This peritrophic matrix serves a variety of functions such as a barrier that protects the epithelium from mechanical damage by food particles, from exposure to large toxin molecules present in food, and also from microbial invasion to an extent. It also aids in concentrating food and digestive enzymes. As it takes 12-30 h for the complete formation of the peritrophic membrane, it does not remain as an intense barrier to filarial worms or parasites which can enter the midgut within few hours of invasion,. Thus, basic architecture of gut can be modified depending on the specialized niche and feeding habits.
Microbial inhabitants of gut
Mosquito as a holobiont undergoes a metamorphic transition from larval to the adult stage. Microbial inhabitants of mosquito and its larvae refer to the microbial communities which colonize in the target organism. The microflora associated with larvae is replaced in the adult mosquito with a new set of microbes. This variation in the microbiota is due to the significant changes in host mosquito according to the changes in the environment and feeding habits. This process of microbial cleaning and acquisition is termed as gut sterilization. During their larval stage mosquito mainly consume bacteria and planktons as nutritive resources. This paves the initial stage of bacterial colonization that adds to resident members. Among the microbes, the bacteria colonize more in the midgut than in salivary gland and reproductive organs,,. Later during adult stages, mosquitoes begin to feed on nectar and blood which triggers the proliferation of some types of microbes and the decline of the other bacteria. Thus, the host diet and its developmental stage plays a crucial role in shaping the gut microbiome. The gut microbiome is generally analysed by dissecting gut of IV instar larvae of field caught or laboratory reared mosquitoes. To enchance the microbial growth the mascerated gut is grown in nutrient media. Later the microbial content are analysed by molecular techniques like pyrosequencing.
The resident communities inside the gut of mosquitoes can vary from microscopic dominant bacteria to even members of Protista [Table 1]. This resident consortium can be changed by the influx of new microbes from their natural habitat. Mosquitoes such as Anopheles, Aedes, and Culex normally lay eggs in water that contains bacteria. The presence of aquatic plants influences the microbial communities as they serve as a larval resource or provide cues for egg-laying adult mosquito, and many microbes of these plants also get transmitted to adult gut trans-steadily,,. These microbes have a significant impact on mosquito life traits like reproduction, fecundity, immunity and vector competence.
As per previous earlier studies, the general bacterial flora in mosquitoes includes gram-negative phylum Proteobacteria (Gammaproteobacteria, Alphaproteobacteria, and Betaproteobacteria) phylum Bacteroidetes, gram-positive phylum Firmicutes including Clostridia, Actinomycetes, Spirochetes, and other species. Naturally, a bacterial community in mosquito gut can reduce the development of Plasmodium, a human parasite (due to the presence of gram-negative bacteria). The outer membrane of the cell wall in these gram-negative bacterial cell wall contains lipopolysaccharides which acts as a physical barrier for harmful agents like hydrogen peroxide etc, while gram-positive bacteria have no such barrier. Furthermore, different gram-negative bacteria have varying effects against Plasmodium. These variations may show certain differences in the production of certain metabolites. For example, red pigment prodigiosin produced by gram-negative bacteria is found to be effective against Plasmodium. One reason for this is the upregulation of immune genes that encode antimicrobial peptides (AMP) and a thioester-containing protein having an antiparasitic effect. These gut resident bacteria can be symbiotic or pathogenic [Table 1]. The symbiotic microbes are beneficial to host in many ways. It includes dietary supplementation, enhancement of in digestive mechanism, and tolerance towards environmental perturbation and protection from the parasite.
Nature of anopheline gut
Genus Anopheles which comprises approximately 550 species is cosmopolitan in distribution. Each mosquito genus has a specific ecological preference for selecting its habitat. For example, genus Anopheles are mostly observed in clear water exposed to direct sunlight. As non-selective filter feeder, Anopheles larvae indiscriminately feed inorganic matter like dust and organic matter such as filamentous algae, fungi, rotifers, cyanobacteria, zooflagellates and crustaceans present in water. They utilize mouth brushes or lateral palatal brushes as paddles to create currents by using energy for ingesting food particles.
The anopheline gut microbiome is strongly influenced by microbes suspended in its natural habitat. This has been proved by the thorough gut analysis of mosquito larvae by Howland who dissected over 1000 larvae of eight species, identified the algae present, and ranked them by abundance in the food. She concluded that the abundance of algae in the larval food is correlated with algal abundance in the habitats. This has been also shown in another study on Anopheles quadrimaculatus larvae, a common vector of malaria in the Eastern United States wherein the elimination of algae from a small pond with copper sulfate demonstrated its absence in their food. However, after recolonization the same pond, algal cells were again observed in the larval gut.
The anopheline gut is dominated by resident bacteria of genus Pantoea and Asaia. These bacteria have shown stable association with anopheline mosquitoes during different life stages. Pantoea, natural mosquito symbiont can cross-colonise several mosquito species and is readily transformed and cultured; this property of Pantoea has been proposed for paratransgenic applications,· Asaia acts as an immunomodulator by producing antimicrobial peptides that interfere with the course of infection particularly its invasion to epithelial tissues and salivary gland.
Recent research on two Anopheles species An. gambiae and An. coluzzii from Ghana compared the midgut microbiota of mosquitoes during rainy and dry seasons from urban and rural breeding sites using 454 pyrosequencing. The data suggested that An. gambiae and An. coluzzi do not differ significantly in their gut microenvironment. Shewanellaceae family was observed in both the species. Bacterial families Enterobacteriaceae and Aeromonadaceae, were also associated with Anopheles mosquitoes. The only difference observed was among An. gambiae collected from the different breeding site during summer. Aeromonas, Shewanella, and Thorsellia were other bacterial genera found to be significantly varying in abundance according to the breeding sites. This indicates that larval breeding site has a significant impact on the adult mosquito midgut composition. The presence of Enterobacter and Serratia strain in Anopheles mosquito gut have an antiparasitic effect on mosquito. Enterobacteriaceae that survived during the rainy season is found to be more in number than that of during the dry season. Two members of this family include Enterobacter species and Thorsellia anopheles. This gram-negative Enterobacter can directly act on Plasmodium falciparum and hinders the development of the parasite. Thorsellia anophelis was the dominant species in the midgut of An. gambiae. This symbiotic association with host mosquito vector attributes to its high tolerance for mosquito midgut alkalinity. Serratia marcescens HB3, isolated from laboratory-reared An. stephensi mosquitoes, inhibits Plasmodium development within the mosquito midgut by interrupting ookinete invasion through the midgut epithelial cells. Phenotypic variation at the cellular and structural levels was observed and directly correlated with the ability to induce resistance against Plasmodium invasion.
The prevailing environmental conditions have a great influence on the gut microbiome and host- vector competence. One such parameter is the influence of chemicals in regulating the bacterial fauna in mosquito gut. For example, Pseudomonas aeruginosa boost the larval development of Culex quinquefasciatus in phosphate-rich medium.
Microbial diversity of gut microbiome in genus Aedes
Aedes, an arbovirus vector of dengue, chikungunya and Zika virus draws special attention due to their rapid geographical spread and increasing disease burden,,. This is due to the association between certain gut microbes and potent human pathogens such as parasite, virus, and bacteria in host vector.
Zouache et al explored the composition and diversity of mosquito-associated bacteria in relation to mosquito habitats from different geographical regions of Madagascar on wild Ae. aegypti and Ae. albopictus. This was done using the traditional culturing method and by denaturing gradient gel electrophoresis (DGGE) and sequencing of rrs amplicons of bacteria. This survey highlighted the variance in the relative abundance and composition of mosquito-associated bacteria during developmental stages. To know the influence of external microorganism with the internal gut microbe, the analyses were done on laboratory-reared and wild targeted population. Wild Aedes gut generally had richer bacterial profile than laboratory reared ones consisting of Serratia marcescens, Klebsiella ozaenae, P. aeruginosa, Enterobacter, Proteobacteria and Flavobacteriaceae species depending upon the stages of development.
Extensive work of Coon et al on Ae. aegypti and Ae. albopictus have shown that the I instar axenic larvae of these species were not able to develop properly in the absence of bacteria; though, they developed normally into adult in laboratory aquatic habitat recolonized with bacteria. Moreover, insect colonized microbial community also protects the host against pathogens. Interesting examples are available from different research reports such as Wolbachia an endosymbiotic resident bacterium in the gut can interfere the replication of chikungunya and dengue virus in Aedes mosquito. This is also supported by another result in which removal of the bacterial community in antibiotic fed Anopheles mosquitoes increases their susceptibility to malaria parasite infection. These observations suggest that the microbial gut flora of insect can be manipulated to control their vectorial capacity.
In India, attempts to survey the midgut microflora have remained mainly focused on two genus, Culex, and Anopheles mosquitoes, which act as vectors for Japanese encephalitis, filariasis, and malaria, , ,,,. In spite of being the major vector for dengue, midgut microbial diversity studies for different species of Aedes mosquitoes are rare from India. One such attempt has been performed on the midgut microbiota of Ae. aegypti and Ae. albopictus from the Arunachal Pradesh. This study, focused on the characterization of culture-dependent aerobic bacteria from the midgut of both species of Aedes mosquitoes, as the culturable bacteria can be used for further applications in the management of disease transmission such as paratrangenesis. The results showed maximum bacterial species of gram-negative Enterobacteriaceae family and gram-positive Bacillaceae family. This study also suggests that mosquito midgut bacteria are primarily inherited through vertical inheritance or through acquisition from the environment. The presence of these gut microbiota is essential for maintaining a fine-tuned balance for existence. This finding is important since in number of studies species belonging to Enterobacter genus has been reported to block the development of P. falciparum in An. gambiae and sporogonic development of P. vivax in An. albimanus,  by inducing the immune responses.
Culex mosquitoes are filter feeders and consume bacteria and many other micro-organisms in the water column. A complex microbial community is a fundamental necessity for the normal survival and complete development of these mosquito larvae to adult. Earlier studies have shown that the microbial communities isolated from the mid-gut of laboratory-reared IV instar Culex tarsalis Coquillett (a vector of Western encephalitis and West Nile viruses) using conventional culturing techniques included several species, like Lactobacillus, Micrococcus, Saccharomyces, Proteus rettgeri, Geotrichum, Pseudomonas, and other unidentified gram-negative bacteria. Among these, Micrococcus species (Actinobacteria), Lactobacillus (Firmicutes : Bacilli) and Pseudomonas (Gammaproteobacteria) are commonly found in Cx. tarsalis guts. Most genera of bacteria found in the gut of larval Cx. tarsalis were also found in the adults, with the exception of Aerobacter, Escherichia, and Flavobacterium.
Research conducted by Muturi et al in 2016 on Cx. pipiens and Cx. restuans, the primary vectors of West Nile encephalitis in Champaign County in the USA by 16S RNA sequencing method provided a comprehensive analysis of microflora in these mosquitoes. It included Proteobactericea, viz. Wolbachia and Spingomonas species; and Firmicutes like Alicyclobcillus species. Even though the members of Proteobactericea dominated in both the species, Cx. restuans had more diverse population.
Like bacteria and virus, eukaryotic fungus is an inmate of mosquito gut microbiome. Its role as a commensal, mutualistic or as pathogenic is inevitable in maintaining ecological balance in mosquitoes. During the metamorphic transition, mosquitoes are exposed to fungi in the form of mosquito larvae in water, or through the ingestion of fungi in sugar meal or by physical contact with conidia (adult mosquitoes). Filamentous fungi and yeast are the common fungal isolates present in the midgut and other tissues of mosquitoes. A filamentous fungus comprises some species of Aspergillus and Penicillium as pathogenic forms and some genera of fungi like Beauveria and Metarhizium as entomopathogenic forms. Different genera of yeast like Candida, Pichia and Wickerhamomyces have been identified in Aedes and Anopheles mosquitoes through culture dependent and culture independent methods. Earlier explorations in mosquito mycodiversity were based on these types of the culture-dependent method. For example, a yeast strain Wickerhamomyces anomalus has been reported in the midgut and reproductive organ of An. stephensi, a primary vector of malaria. Recently, with the advent of high throughout sequencing (HTS) technique, the knowledge about mosquito mycobiome has widened. This HTS technique was employed to analyze the mycobial composition in Ae. triseriatus and Ae. japanicum. The sequence revealed the presence of 21 distinct fungal operational taxonomic units (OTUs), out of which 15 were shared between these two species. Ascomycota phylum is the major fungal taxa in these two Aedes species. Even though the presence of mycobiome is evident in mosquito, a little is known about the tripartite interaction between vector, pathogen, and fungi.
Mosquito act as an exclusive host for a large group of virus which are insect-specific,. A metagenomic approach was used to evaluate viral load by Shi et al in two genera of mosquitoes Aedes and Culex. The comparison presented a striking difference in the virome of mosquitoes, where in genus Aedes showed a low viral diversity and less abundance than Culex. This metagenomic approach lead to the identification/discovery of different viral families in mosquitoes such as Bunyaviridae, Rhabdoviridae, Orthomyxoviridae, Flaviviridae, Mesoviridae, Reoviridae, and unclassified Chuvirus, and Negevirus groups. Most resident virome act as commensal microbe due to its inability to infect vertebrate cell lines, prolonged host infection and vertical transmission.
Influence of microbes on host vectorial capacity
Vectorial capacity is a quantitative measure of several factors like cellular, biochemical, behavioural, immunological, genetic and environmental parameters which can influence vector density, longevity and vector competence. All these factors are interrelated and can determine the pathogenicity and nonpathogenecity in mosquitoes.
Bacteria, a dominant member of gut microflora may interact directly or indirectly with invading pathogens. The indirect interaction is by activating innate immune response, . Normally pattern recognition receptors (PRRS) on the host cell recognizes the conserved surface determinants called pathogen associated molecular patterns (PAMPs) exclusively present/found in microbes. This binding triggers immune signaling pathways such as the toll pathway or the immune deficiency (IMD) pathway. In toll cell signaling pathway a cascade of events leads to the degradation of IF-ƙB like transcription factor (Cactus), nuclear translocation of NF-ƙB like transcription factors (Dif and Dorsal) that leads to the expression of antimicrobial peptides (AMP) genes. This AMP, produced in the fat body is secreted into haemolymph, where they directly kill the invading microorganism. Genetic analysis has revealed that the AMP gene expressions are mainly controlled by the toll pathway and IMD pathway. The toll pathway is mainly activated by gram-positive bacteria, human P. falciparum, and DENV. The presence of gram-negative bacteria activates the IMD pathway which controls antibacterial peptide gene control.
Application of microbes in mosquito vector control
Vector-borne diseases are spreading at an alarming rate. The traditional control strategies have achieved some progress in malaria control, but the incidence of arboviral diseases are on rise. The insecticide resistance among vectors and lack of vaccines are the two important reasons for this pandemic,. So, the need of novel control strategies is essential to check emerging and re-emerging pathogens. In this regard, microbial based intervention is gaining due importance as a novel remedy to control these diseases.
Genus Wolbachia is an endosymbiotic, gram-negative, Alphaproteobacteria within the family Rickettsiaceae. Wolbachia strain has the capacity of cytoplasmic incompatibility (CI) which leads to production of sterile offspring, when an uninfected female mates with the Wolbachia-infected male mosquitoes. CI can also occur when mating occurs between mosquitoes infected with different, incompatible Wolbachia strains. This quality of Wolbachia has been exploited to control target vector mosquitoes by transinfection methods. The Wolbachia strain wMelPop present in Drosophila melanogaster has the quality to dramatically shorten the host longevity.
Enterobacter species are common gram-negative bacterial inhabitant present in genus Aedes, Culex and Anopheles. These bacterial strains produce reactive oxygen species that affect the development of oocyst from ookinetes. The reactive oxygen species interferes with the development of parasite leading to its death before its invasion to the intestinal environment.
Bacillus thuringiensis (Berliner) serovariety israelensis (Bti) de Barjac and strains of Bacillus spherical Neide are used as a nonchemical method to control mosquitoes. It is a gram-positive spore forming bacteria observed in soil, aquatic areas, dead insects, grains etc,,,, 81-86. They secrete delta endotoxin which has the capacity to kill the host organism. These principles are used to modify bacteria to kill disease-causing vectors.
Paratransgenesis, a new technique that attempts to eliminate a pathogen from vector populations through transgenesis of a symbiont of the vector has gained special attention. In this approach, microbes that reside within the gut of vectors are engineered to secrete anti-pathogen molecules. Asaia an Alphaproteobacteria, present in all the developmental stages of host, in different regions (of host) make it an ideal choice for paratransgenesis,,. Attempts have been made to modify more strains of Asaia to secrete antiplasmodium effector molecules against malaria.
Entomopathogenic fungi can be used as a potential biological weapons agent against vector control. Normally spores or conidia which germinate on mosquito surface penetrate through the cuticle and reaches the haemolymph. Beauveria bassiana and Metarhizium anisoplia are naturally occurring filamentaous fungi. Beauveria bassiana produces a toxin oosporein, which downregulate Duox expression in host midgut, and thereby slowly kills the mosquitoes. This slow killing process is an added advantage because it results in slow selective pressure for resistance, reduction in reproductive fitness, and prevent pathogenic transmission of vector.
| Conclusion|| |
The mosquito gut is inhabited by a large number of microbes. Understanding the symbiotic relationship between the gut microbiome and the host mosquito can facilitate novel intervention strategies for mosquito vector control. Paratransgenic strategy, wherein the symbiotic or commensal microbes of host mosquitoes/insects are genetically altered to express gene products that interfere with pathogen transmission, could act as valuable tool for control of vector-borne diseases. Bacteria, fungi and virus can be used as excellent candidates for paratransgenesis. This approach limits the adverse effects of many insecticides on nontarget species including humans, environment, soil and water; and also avert development of mosquito resistance. The tiny nature of densovirus remain as an attractive option to use it as a transgene with improved killing efficiency and capacity to reduce selective pressure for resistance to control mosquito population. Enhancing the ability of resident entamopathogenic fungi to shorten the mosquito life span by genetic manipulation also appears viable.
Techniques like introduction of Wolbachia in natural populations of mosquito, use of Bti strains, etc. are other promising vector control strategies. Knowledge and ability to manipulate the microbial diversity in mosquitoes can be potentially used to alter their competence and survival, as microbes have several desirable properties for applied control strategies, particularly the ability to disseminate through vector populations. The antipathogenic capacity of the microbes needs vast exploration to discover a breakthrough method of controlling disease transmission.
Conflict of interest
The authors declare that they have no conflict of interest.
| Acknowledgements|| |
The authors are thankful to the Principal, St. Joseph's College for providing the necessary laboratory facilities, and gratefully acknowledge the University Grants Commission, New Delhi for providing funds under UGC Research Award.
| References|| |
Trari B, Dakki M, Harbach RE. An updated checklist of the Culicidae (Diptera) of Morocco, with notes on species of historical and current medical importance. J Vector Ecol
Bhattacharyya D, Rajavel A, Mohapatra P, Jambulingam P, Mahanta J, Prakash A. Faunal richness and the checklist of Indian mosquitoes (Diptera: Culicidae). Check List
2014; 10(6): 1342-58.
Bandyopadhyay S, Lum L, Kroeger A. Classifying dengue: A review of the difficulties in using the WHO case classification for dengue haemorrhagic fever. Trop Med Int Health
Bhatt S, Weiss D, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al
. The effect of malaria control on Plasmodium falciparum
in Africa between 2000 and 2015. Nature
2015; 526(7572): 207.
Moll RM, Romoser WS, Modrakowski MC, Moncayo AC, Lerdthusnee K. Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J Med Entomol
2001; 38(1): 29-32.
Chandel K, Mendki MJ, Parikh RY, Kulkarni G, Tikar SN, Sukumaran D, et al
. Midgut microbial community of Culex quinquefasciatus
mosquito populations from India. PLoS One
2013; 8(11): e80453.
|9.|Biological control of mosquitoes
. In: Chapman HC, editor. Fresno, CA, USA: American Mosquito Control Association 1985. Bull Am Mosq Control Assoc
No. 6, 1985; p. 218.
Wang Y, Gilbreath III TM, Kukutla P, Yan G, Xu J. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae
in Kenya. PloS One
2011; 6(9): e24767.
Merritt R, Dadd R, Walker E. Feeding behaviour, natural food, and nutritional relationships of larval mosquitoes. Ann Rev Entomol
1992; 37(1): 349-74.
Cruden D, Markovetz A. Microbial ecology of the cockroach gut. Ann Rev Microbiol
1987; 41(1): 617-43.
Chapman RF. The insects: Structure and function. V edn. In: Terblanche J, Simpson S, Douglas A, editors. United Kingdom: Cambridge University Press 2013.
Peters W, Wiese B. Permeability of the peritrophic membranes of some Diptera to labelled dextrans. J Insect Physiol
Spence KD, Kawata MY. Permeability characteristics of the peritrophic membranes of Manduca sexta
larvae. J Insect Physiol
1993; 39(9): 785-90.
Ferreira C, Capella AN, Sitnik R, Terra WR. Properties of the digestive enzymes and the permeability of the peritrophic membrane of Spodoptera frugiperda
(Lepidoptera) larvae. Comp Biochem Physiol
Barbehenn RV, Martin MM. Permeability of the peritrophic envelopes of herbivorous insects to dextran sulfate: A test of the polyanion exclusion hypothesis. J Insect Physiol
Edwards MJ, Jacobs-Lorena M. Permeability and disruption of the peritrophic matrix and caecal membrane from Aedes aegypti
and Anopheles gambiae
mosquito larvae. J Insect Physiol
Al-Olayan EM, Williams GT, Hurd H. Apoptosis in the malaria protozoan, Plasmodium berghei:
A possible mechanism for limiting intensity of infection in the mosquito. Int J Parasitol
2002; 32(9): 1133-43.
Lehane M. Peritrophic matrix structure and function. Ann Rev Entomol
1997; 42(1): 525-50.
Shao L, Devenport M, Jacobs-Lorena M. The peritrophic matrix of hematophagous insects. Archives Insect Biochem Physiol
2001; 47(2): 119-25.
Ponnudurai T, Billingsley P, Rudin W. Differential infectivity of Plasmodium
for mosquitoes. Parasitol Today
1988; 4(11): 319-21.
Zouache K, Raharimalala FN, Raquin V, Tran-Van V, Raveloson LHR, Ravelonandro P, et al
. Bacterial diversity of field-caught mosquitoes, Aedes albopictus
and Aedes aegypti
, from different geographic regions of Madagascar. FEMS Microbiol Ecol
2010; 75(3): 377-89.
Noden BH, Vaughan JA, Pumpuni CB, Beier JC. Mosquito ingestion of antibodies against mosquito midgut microbiota improves conversion of ookinetes to oocysts for Plasmodium falciparum
, but not P. yoelii. Parasitol Int
2011; 60(4): 440-6.
Oliveira JHM, Gonçalves RL, Lara FA, Dias FA, Gandara ACP, Menna-Barreto RF, et al
. Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti
and allows proliferation of intestinal microbiota. PLoS Pathog
2011; 7(3): e1001320.
Gusmão DS, Santos AV, Marini DC, Bacci M Jr, Berbert-Molina MA, Lemos FJA. Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti
(Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Trop
2010; 115(3): 275-81.
Jadin J, Vincke I, Dunjic A, Delville J, Wery M, Bafort J, et al
. Role of Pseudomonas in the sporogenesis of the hematozoon of malaria in the mosquito. Bull Soc Pathol Exot Filiales
1966; 59(4): 514-25.
Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC. Bacterial population dynamics in three anopheline species: The impact on Plasmodium
sporogonic development. Am J Trop Med Hyg
1996; 54(2): 214-8.
Briones AM, Shililu J, Githure J, Novak R, Raskin L. Thorsellia anophelis
is the dominant bacterium in a Kenyan population of adult Anopheles gambiae
mosquitoes. ISME J
2008; 2(1): 74-82.
Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA, et al
. Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi:
A step toward finding suitable paratransgenesis candidates. Acta Trop
2012; 121(2): 129-34.
Kumar S, Molina-Cruz A, Gupta L, Rodrigues J, Barillas-Mury C. A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science
2010; 327(5973): 1644-8.
Favia G, Ricci I, Damiani C, Raddadi N, Crotti E, Marzorati M, et al
. Bacteria of the genus Asaia
stably associate with Anopheles stephensi
, an Asian malarial mosquito vector. Proc Natl Acad Sci
2007; 104(21): 9047-51.
Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A, Scuppa P, et al
. Paternal transmission of symbiotic bacteria in malaria vectors. Curr Biol
2008; 18(23): R1087-8.
Damiani C, Ricci I, Crotti E, Rossi P, Rizzi A, Scuppa P, et al
. Mosquito-bacteria symbiosis: The case of Anopheles gambiae
and Asaia. Microbial Ecol
2010; 60(3): 644-54.
Cirimotich CM, Dong Y, Clayton AM, Sandiford SL, Souza-Neto JA, Mulenga M, et al
. Natural microbe-mediated refractoriness to Plasmodium
infection in Anopheles gambiae. Science
2011; 332(6031): 855-8.
Lindh JM, Terenius O, Faye I. 16S rRNA gene-based identification of midgut bacteria from field-caught Anopheles gambiae sensu lato
and An. funestus
mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol
2005; 71(11): 7217-23.
Mulligan III FS, Schaefer CH, Wilder WH. Efficacy and persistence of Bacillus sphaericus
and B. thuringiensis
H 14 against mosquitoes under laboratory and field conditions. J Econ Entomol
1980; 73(5): 684-8.
Mulligan III FS, Schaefer CH. Integration of a selective mosquito control agent Bacillus thuringiensis
serotype H-14, with natural predator populations in pesticide-sensitive habitats. Proceedings and Papers of Annual Conference
held at California from 26–29 April 1981. California, USA: Mosquito and Vector Control Association 1981; p. 19-22.
Mulla M, Chaney J, Rodcharoen J. Elevated dosages of Bacillus thuringiensis
fail to extend control of Culex
larvae. Bull Soc Vect Ecol
Mulla MS, Thavara U, Tawatsin A, Chomposri J, Su T. Emergence of resistance and resistance management in field populations of tropical Culex quinquefasciatus
to the microbial control agent Bacillus sphaericus. J Am Mosq Control Assoc
2003; 19(1): 39-46.
Pidiyar VJ, Jangid K, Patole MS, Shouche YS. Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus
mosquito midgut based on 16S ribosomal RNA gene analysis. Am J Trop Med Hyg
2004; 70(6): 597-603.
Fragkoudis R, Attarzadeh-Yazdi G, Nash AA, Fazakerley JK, Kohl A. Advances in dissecting mosquito innate immune responses to arbovirus infection. J General Virol
Favia G, Ricci I, Marzorati M, Negri I, Alma A, Sacchi L, et al
. Bacteria of the genus Asaia:
A potential paratransgenic weapon against malaria. Transgenesis and the management of vector-borne disease
. London: Springer 2008; p. 49-59.
Ren X, Hoiczyk E, Rasgon JL. Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog
Fang W, Vega-Rodríguez J, Ghosh AK, Jacobs-Lorena M, Kang A, Leger RJS. Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science
2011; 331(6020): 1074-7.
Clements A. Sensory, reception and behavior. Biol Mosq
Chukalo E, Abate D. Bacterial populations of mosquito breeding habitats in relation to maize pollen in Asendabo, southwestern Ethiopia. African J Microbiol Res
Howland LJ. Bionomical investigation of English mosquito larvae with special reference to their algal food. J Ecol
1930; 18(1): 81-125.
Coggeshall LT. Relationship of plankton to anopheline larvae. Am J Hyg
1926; 6(4): 556-69.
Bisi DC, Lampe DJ. Secretion of anti-Plasmodium
effector proteins from a natural Pantoea agglomerans
isolate by using PelB and HlyA secretion signals. Appl Environ Microbiol
2011; 77(13): 4669-75.
Djadid ND, Jazayeri H, Raz A, Favia G, Ricci I, Zakeri S. Identification of the midgut microbiota of An. stephensi
and An. maculipennis
for their application as a paratransgenic tool against malaria. PLoS One
2011; 6(12): e28484.
Akorli J, Gendrin M, Pels NAP, Yeboah-Manu D, Christophides GK, Wilson MD. Seasonality and locality affect the diversity of Anopheles gambiae
and Anopheles coluzzii
midgut microbiota from Ghana. PloS One
2016; 11(6): e0157529.
Bando H, Okado K, Guelbeogo WM, Badolo A, Aonuma H, Nelson B, et al
. Intra-specific diversity of Serratia marcescens
mosquito midgut defines Plasmodium
transmission capacity. Sci Rep
Peck GW, Walton WE. Effect of bacterial quality and density on growth and whole body stoichiometry of Culex quinquefasciatus
and Culex tarsalis
(Diptera: Culicidae). J Med Entomol
2006; 43(1): 25-33.
Christophers SR. Aedes aegypti
(L.) the yellow fever mosquito: Its life history, bionomics and structure. London: Cambridge University Press 1960; p. 752.
Mattingly P. Genetical aspects of the Aëdes aegypti
problem: I—Taxonom and bionomics. Ann Trop Med Parasitol
Mattingly P. Taxonomy of Aedes aegypti
and related species. Bull World Health Organ
1967; 36(4): 552-4.
Rani A, Sharma A, Rajagopal R, Adak T, Bhatnagar RK. Bacterial diversity analysis of larvae and adult midgut microflora using culture-dependent and culture-independent methods in lab-reared and field-collected Anopheles stephensi
–An Asian malarial vector. BMC Microbiol
2009; 9(1): 96.
Coon KL, Brown MR, Strand MR. Gut bacteria differentially affect egg production in the anautogenous mosquito Aedes aegypti
and facultatively autogenous mosquito Aedes atropalpus
(Diptera: Culicidae). Parasit Vectors
2016; 9(1): 375.
Dong Y, Manfredini F, Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog
2009; 5(5): e1000423.
Chandel K, Parikh RY, Mendki MJ, Shouche YS, Veer V. Isolation and characterization of Vagococcus
sp from midgut of Culex quinquefasciatus
(Say) mosquito. J Vector Borne Dis
2015; 52(1): 52.
Pal A, Rai C, Roy A, Banerjee PK. Studies on midgut microbiota of wild caught Culex (Culex quinquefasciatus)
mosquitoes from Barasat (North 24 Parganas) of West Bengal. Int J Mosq Res
2014; 1(2): 41-7.
Yadav KK, Bora A, Datta S, Chandel K, Gogoi HK, Prasad G, et al
. Molecular characterization of midgut microbiota of Aedes albopictus
and Aedes aegypti
from Arunachal Pradesh, India. Parasit Vectors
2015; 8(1): 641.
Gonzalez-Ceron L, Santillan F, Rodriguez MH, Mendez D, Hernandez-Avila JE. Bacteria in midguts of field-collected Anopheles albimanus
block Plasmodium vivax
sporogonic development. J Med Entomol
2003; 40(3): 371-4.
Christophers SR. The fauna of British India including Ceylon and Burma
. London, UK: Taylor and Francis 1933.
Muturi EJ, Kim C-H, Bara J, Bach EM, Siddappaji MH. Culex pipiens
and Culex restuans
mosquitoes harbor distinct microbiota dominated by few bacterial taxa. Parasit Vectors
2016; 9(1): 18.
Lynch PA, Grimm U, Thomas MB, Read AF. Prospective malaria control using entomopathogenic fungi: Comparative evaluation of impact on transmission and selection for resistance. Malar J
Scholte E-J, Knols BG, Samson RA, Takken W. Entomopathogenic fungi for mosquito control: A review. J Insect Sci
Ricci I, Damiani C, Scuppa P, Mosca M, Crotti E, Rossi P, et al
. The yeast Wickerhamomyces anomalus (Pichia anomala)
inhabits the midgut and reproductive system of the Asian malaria vector Anopheles stephensi. Environ Microbiol
2011; 13(4): 911-21.
Muturi EJ, Bara JJ, Rooney AP, Hansen AK. Midgut fungal and bacterial microbiota of Aedes triseriatus
and Aedes japonicus
shift in response to La Crosse virus infection. Mol Ecol
2016; 25(16): 4075-90.
Bolling BG, Weaver SC, Tesh RB, Vasilakis N. Insect-specific virus discovery: Significance for the arbovirus community. Viruses
2015; 7(9): 4911-28.
Vasilakis N, Tesh RB. Insect-specific viruses and their potential impact on arbovirus transmission. Curr Opin Virol
Shi M, Neville P, Nicholson J, Eden J-S, Imrie A, Holmes EC. High-resolution metatranscriptomics reveals the ecological dynamics of mosquito-associated RNA viruses in Western Australia. J Virol
2017; 91(17): e00680-17.
Beerntsen BT, James AA, Christensen BM. Genetics of mosquito vector competence. Microbiol Mol Biol Rev
Kingsolver MB, Huang Z, Hardy RW. Insect antiviral innate immunity: Pathways, effectors, and connections. J Mol Biol
2013; 425(24): 4921-36.
Christophides GK, Vlachou D, Kafatos FC. Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol Rev
2004; 198(1): 127-48.
Naqqash MN, Gökçe A, Bakhsh A, Salim M. Insecticide resistance and its molecular basis in urban insect pests. Parasitol Res
2016; 115(4): 1363-73.
Ranson H, Lissenden N. Insecticide resistance in African Anopheles
mosquitoes: A worsening situation that needs urgent action to maintain malaria control. Trends Parasitol
2016; 32(3): 187-96.
Werren JH, Baldo L, Clark ME. Wolbachia:
Master manipulators of invertebrate biology. Nat Rev Microbiol
2008; 6(10): 741.
Min K-T, Benzer S. Wolbachia
, normally a symbiont of Drosophila
, can be virulent, causing degeneration and early death. Proc Natl Acad Sci
1997; 94(20): 10792-6.
Martin PA, Travers RS. Worldwide abundance and distribution of Bacillus thuringiensis
isolates. Appl Environ Microbiol
1989; 55(10): 2437-42.
Smith RA, Couche GA. The phylloplane as a source of Bacillus thuringiensis
variants. Appl Environ Microbiol
1991; 57(1): 311-5.
Beegle CC, Yamamoto T. Invitation paper (CP Alexander Fund): History of Bacillus thuringiensis
Berliner research and development. The Canadian Entomologist
1992; 124(4): 587-616.
Meadows M. Bacillus thuringiensis
in the environment: Ecology and risk assessment. Theory Prac
1993; p. 193-220.
Damgaard PH. Natural occurrence and dispersal of Bacillus thuringiensis
in the environment. In: Charles JF, Delecluse A, Nielsen Le, Roux C, editors. Entomopathogenic bacteria: From laboratory to field application
. Netherlands: Springer 2000; p. 23-40.
Glare TR, O’callaghan M. Bacillus thuringiensis:
Biology, ecology and safety. Chichester, New York: Wiley 2000; p. 368.
Wei G, Lai Y, Wang G, Chen H, Li F, Wang S. Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality. Proc Natl Acad Sci
2017; 114(23): 5994-9.
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