The mosquito holobiont: fresh insight into mosquito-microbiota interactions

Abstract

The holobiont concept was first developed for coral ecosystems but has been extended to multiple organisms, including plants and other animals. Studies on insect-associated microbial communities have produced strong evidence that symbiotic bacteria play a major role in host biology. However, the understanding of these symbiotic relationships has mainly been limited to phytophagous insects, while the role of host-associated microbiota in haematophagous insect vectors remains largely unexplored. Mosquitoes are a major global public health concern, with a concomitant increase in people at risk of infection. The global emergence and re-emergence of mosquito-borne diseases has led many researchers to study both the mosquito host and its associated microbiota. Although most of these studies have been descriptive, they have led to a broad description of the bacterial communities hosted by mosquito populations. This review describes key advances and progress in the field of the mosquito microbiota research while also encompassing other microbes and the environmental factors driving their composition and diversity. The discussion includes recent findings on the microbiota functional roles and underlines their interactions with the host biology and pathogen transmission. Insight into the ecology of multipartite interactions, we consider that conferring the term holobiont to the mosquito and its microbiota is useful to get a comprehensive understanding of the vector pathosystem functioning so as to be able to develop innovative and efficient novel vector control strategies.

Keywords: Adaptation; Mosquito; Multiple interactions; Pan-microbiota; Pathogen transmission; Symbiosis.

Fig. 1

Venn diagrams illustrating overlapping of bacterial composition between mosquito species, development stages and habitats. a Number of bacterial taxa specific and common between mosquito larvae, habitats and adults of Aedes japonicus, Aedes triseriatus and Anopheles gambiae [20, 21]. b Number of bacterial taxa specific and common to larvae of Anopheles gambiae, Culex pipiens, Culex nigripalpus, Aedes aegypti and Aedes japonicus [17, 18, 20, 22, 23, 27]. c Number of bacterial taxa specific and common to adults of Anopheles gambiae, Anopheles stephensi, Culex nigripalpus, Aedes albopictus and Aedes aegypti [, , , , , , , –, –37, 39]. An additional table shows in more detail the identification of bacterial species/genera in mosquito species [see Additional file 1]

Fig. 2

Putative functions of mosquito-associated microbiota (bacteria and fungi). Functions related to metabolism are indicated in orange and those related to life history traits are indicated in yellow: (1) Blood digestion (Acinetobacter, Pantoea, Enterobacter, Dysgonomonas), (2) Sugar digestion (Acinetobacter, Elizabethkingia, Thorsellia, Sphingomonadaceae family, Meyerozyma), (3) Supply of vitamins and amino acids (Dysgonomonas, Klebsiella, Aeromonas, Saccharomyces cerevisiae), (4) Survival (Escherichia coli, Beauveria bassiana), (5) Mediating oviposition site choice (Klebsiella, Aeromonas), (6) Egg production (Comamonas), (7) Larval development (Acinetobacter, Asaia, Aeromonas, Chryseobacterium, Paenibacillus, Aquitalea, Escherichia coli) [, , , –75, 77, 80]. Pictures from JM Hosatte, with permission