Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee

Abstract

Horizontal gene transfer (HGT) involves the nonsexual transmission of genetic material across species boundaries. Although often detected in prokaryotes, examples of HGT involving animals are relatively rare, and any evolutionary advantage conferred to the recipient is typically obscure. We identified a gene ( HhMAN1 ) from the coffee berry borer beetle, Hypothenemus hampei , a devastating pest of coffee, which shows clear evidence of HGT from bacteria. HhMAN1 encodes a mannanase, representing a class of glycosyl hydrolases that has not previously been reported in insects. Recombinant HhMAN1 protein hydrolyzes coffee berry galactomannan, the major storage polysaccharide in this species and the presumed food of H. hampei . HhMAN1 was found to be widespread in a broad biogeographic survey of H. hampei accessions, indicating that the HGT event occurred before radiation of the insect from West Africa to Asia and South America. However, the gene was not detected in the closely related species H. obscurus (the tropical nut borer or “false berry borer”), which does not colonize coffee beans. Thus, HGT of HhMAN1 from bacteria represents a likely adaptation to a specific ecological niche and may have been promoted by intensive agricultural practices.

Evolutionary origin of insect– Wolbachia nutritional mutualism

“…Recent studies have revealed that lateral gene transfers sometimes entail evolutionary consequences to adaptive ecological and physiological traits in insects and other organisms (37)(38)(39)(40). Wolbachia endosymbionts occur ubiquitously (7) and rampantly exchange their genetic materials with their cosymbionts and hosts (25,41).…”

The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer

“…As an example, plant-parasitic nematodes have acquired genes encoding PCWDEs from several families; these genes, after further duplication events, have promoted their ability to parasitize plants [3]. Although we suggested in our previous work the possibility that genes encoding PCWDEs in phytophagous beetles may have arisen from HGT events [22] similar to plant-parasitic nematodes, only recently was the first strongly supported case of a functional and adaptive HGT of a mannanase gene in the coffee berry borer, Hypothenemus hampei, reported [23]. Larvae of the coffee berry borer feed exclusively inside coffee berries, which are primarily composed of polysaccharides including a high proportion of mannan.…”

“…HGTs of TEs between several eukaryotes have also been reported [37]. Taking this into account and noting the association between HhMAN1 and TEs, Acuna et al [23] proposed that one component of the remaining elusive mechanism of bacteria-to-animal HGTs could be the transposon-mediated incorporation of foreign DNA. This would be conceivable only if the TEs associated with HhMAN1-or, in our case gh11-1 and gh11-2-have some similarities with prokaryotic-derived ones [38].…”

“…The HhMAN1 gene is flanked by TEs of the Tc1/mariner and hAT superfamilies [23]. TEs are often associated with genome recombination, mobilization and reorganization.…”

The coffee berry borer: the centenary of a biological invasion in Brazil

“…Similarly, a better understanding of the microbiota associated with the coffee berry borer might reveal novel pest management options, including interference with Wolbachia (an α-proteobacterium responsible for female-biased sex ratios) (Vega et al, 2002). The recent identification of a bacterial gene [HhMAN1] from the H. hampei genome, suggests the presence of symbiotic bacteria in the intestinal flora, which allow the insect to use galactomannans present in the coffee seeds (Acuña et al, 2012). We presume that the presence of symbionts might be responsible for allowing H. hampei to occupy a unique ecological niche inside the coffee seeds.…”