the bedbug genome and their bloody habits

Once upon a time, I wrote about traumatic insemination in bedbugs. (Those of my friends who are still traumatised by learning about the reproductive habits of various slug species may not wish to follow that link.) Now, two papers just published in Nature Communications describe the results of sequencing & examining the genome of the common bedbug, Cimex lectularius

Bedbugs have probably been with us since humans first lived in caves, where the bugs jumped (possibly literally) from bats to Homo. They're now a widespread human ectoparasite (found on every continent apart from Antarctica) and have developed resistance to the pesticides once used to control their populations. In introducing their paper on their analysis of the C.lectularius genome, Rosenfeld & his colleagues (2016) comment that

There is a limited molecular understanding of the biology of the bed bug before, during and after feeding on human blood, which is essential to their life cycle since bed bugs are temporary ectoparasites, whereby they access their hosts for blood feeding and then seek the refuge of the indoor environment for digestion, waste production and mating.

To increase our understanding of the bugs' life cycle, Rosenfeld's team looked not only at the genome sequence but at changes in gene expression, finding the most pronounced changes occurred after the insect had sucked its fill of human blood. They also found that these changes in expression 

included genes from the Wolbachia endosymbiont, which shows a simultaneous and coordinated host/commensal response to haematophagous activity. 

In other words, gene expression in both host and parasite changes in a synchronous way after the bug has fed. (Just as an aside, Wolbachia is a bacterium that has a significant impact on the reproductive lives of its host.) In the bugs the change could be described as huge: "20% of all stage-regulated genes" showed differential changes in expression after a blood meal.

As you'd expect, the bugs have a number of genes with anticoagulant activity – after all, having blood coagulate in their needle-like mouthparts while feeding would really gum things up – plus other genes associated with blood-feeding. The research team also identified a number of mutations that confer resistance to pesticides such as pyrethroids & cyclodienes, plus others that may underlie metabolic changes that speed up detoxification. Genes that have an impact on the thickness of the bugs' cuticle also have an impact on resistance (also noted by Benoit et al. 2016). 

In the second paper, Benoit and his colleagues (2016) also analysed the common bedbug genome to produce

a comprehensive representation of genes that are linked to traumatic insemination, a reduced chemosensory repertoire of genes related to obligate hematophagy, host–symbiont interactions, and several mechanisms of insecticide resistance.

Traumatic insemination involves male bugs stabbing their sexual partners pretty much anywhere on their bodies with a sharp, pointy, penis. It's a habit that can lead to the females picking up a range of pathogens, and unsurprisingly natural selection has driven the evolution of a range of adaptations minimising the physical harm and risk of infection. 

Because the bugs are obligate blood-feeders (haematophagous), their chemosensory system has evolved to allow them to find their particular hosts (ie us). The team observed that the genes involved in this system differed between C.lectularius & the related species that feeds on bat blood, as the 2 species have specialised on different hosts. They identified a total of 102 genes involved in chemosensory pathways, well down on the number found in related bugs (hemipterans) that feed on a range of plant species. (On the other hand, they have a much-expanded repertoire of salivary enzymes, compared to the plant-sucking bugs.)

The bedbugs' specialisation on human blood as their sole food source did have some potential pitfalls, as apparently vertebrate blood lacks some of the micronutrients that arthropods require. And that's where Wolbachia comes back into the story: 

such specialization also drives obligate associations with symbionts, including Wolbachia, that generate critical micronutrients that are deficient in vertebrate blood (Benoit et al., 2016).

Wolbachia does this by providing its host with 

a cocktail of specific B vitamins that are critical for reproduction and development

The research team also found genes encoding proteins (aquaporins) that allow the bugs to rapidly shed the excess water imbibed in a blood meal, and concluded that differential expression of aquaporin genes (and others) allow the bugs to survive periods of starvation and dehydration in between hosts.

In their conclusion, Benoit et al. comment that the wealth of information uncovered by these genomic studies may allow us to move towards an answer to a pressing question: 

What triggered the current bed bug resurgence?

To which harassed travellers would probably add, and how can we bring them back under control?

J.B.Benoit, Z.N.Adelman, K.Reinhardt, A.Dolan, M.Poelchau, E.C.Jennings, E.M.Szuter, R.W.Hagan, H,Gujar, J.N.Shukla, F,Zhu, M.Mohan, D.R.Nelson, A.J.Rosendale, C.Derst, V.Resnik, S.Wernig, P.Menegazzi, C.Wegener, N.Peschel et al. (2016) Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nature Communications 7 Article number 10165 doi:10.1038/ncomms10165

J.A.Rosenfeld,D.Reeves, M.R.Brugler, A.Narechania, S.Simon, R.Durrett ,J.Foox, K.Shianna, M.C.Schatz, J.Gandara, E.Afshinnekoo, E.T.Lam, A.R.Hastie, S.Chan, H.Cao, M. Saghbini, A.Kentsis, P.J.Planet, V.Kholodovych, M.Tessler et al. (2016) Genome assembly and geospatial phylogenomics of the bed bug Cimex lectularius.  Nature Communications 7 Article number: 10164 doi:10.1038/ncomms10164

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