Expansions of key protein families in the German cockroach highlight the molecular basis of its remarkable success as a global indoor pest

Abstract

The German cockroach, Blattella germanica, is a worldwide pest that infests buildings, including homes, restaurants, and hospitals, often living in unsanitary conditions. As a disease vector and producer of allergens, this species has major health and economic impacts on humans. Factors contributing to the success of the German cockroach include its resistance to a broad range of insecticides, immunity to many pathogens, and its ability, as an extreme generalist omnivore, to survive on most food sources. The recently published genome shows that B. germanica has an exceptionally high number of protein coding genes. In this study, we investigate the functions of the 93 significantly expanded gene families with the aim to better understand the success of B. germanica as a major pest despite such inhospitable conditions. We find major expansions in gene families with functions related to the detoxification of insecticides and allelochemicals, defense against pathogens, digestion, sensory perception, and gene regulation. These expansions might have allowed B. germanica to develop multiple resistance mechanisms to insecticides and pathogens, and enabled a broad, flexible diet, thus explaining its success in unsanitary conditions and under recurrent chemical control. The findings and resources presented here provide insights for better understanding molecular mechanisms that will facilitate more effective cockroach control.

Evidence for reduced immune gene diversity and activity during the evolution of termites

“…But it is possible that the pleiotropic function of newly evolved fungicidal molecules, like GNBP2(Bulmer et al, 2012), which acts synergistically with the AMP termicin(Velenovsky et al, 2016) may have led to functional redundancy and subsequent loss of drosomycin. Alongside evidence of expanded antioxidant genes in cockroaches (Harrison et al, 2018), our observation of contracted TPX ( a type of peroxidase known as peroxiredoxins (Radyuk et al, 2001)) in the MCRA of higher termites suggested an important link between antioxidant processing and termite evolution. In addition, we found that CTL, comprising a large proportion of hemolymph lipopolysaccharide-binding proteins (LPSBP) underwent two significant contractions in the MRCA of Cryptocercus and termites as well as in the MRCA of Rhinotermitidae and Termitidae.…”

“…In bees, immune gene depletion seems to have preceded the evolution of eusociality(Barribeau et al, 2015), indicating that immune gene family evolution in Hymenoptera is unrelated to evolutionary transitions in sociality. Although the pattern of immune gene diversity loss in early branching termites appears to contrast with this finding, the significant expansions of genes, including immune genes, in cockroaches compared to other non-social insects (Harrison et al, 2018;Li et al, 2018) could be interpreted as a relative enhancement of immune gene diversity in the ancestral cockroach clade followed by a return to a more representative level of gene diversity in termites.…”

“…CTLs play an important role in insect innate immunity and can impact infection outcomes for a range of infectious pathogens as well as regulating host microbiota (Zhu et al, 2020). LPSBPs are significantly expanded in cockroaches (Harrison et al, 2018)and are thought to function as opsonins, by binding the surface molecules of invading microorganisms (Jomori et al, 1990;Jomori and Natori, 1991;Jomori and Natori, 1992). A CTL from the hemolymph of P. americana has been shown to possess phenoloxidase activity (Arumugam et al, 2017;Chen et al, 1995).…”

Blattella germanica displays a large arsenal of antimicrobial peptide genes

“…The main reasons were that the presence of several blattellicin genes and the long Glx-rich regions drastically affected the assembly of the transcriptome. This fact probably took place during the assembly and annotation of B. germanica genome 5,6 .…”

The first cockroach genome and its significance for understanding development and the evolution of insect eusociality

“…Here, a bifurcation seems to have taken place: On the one hand, one group of roaches (termites) has gradually co‐opted many receptors and the corresponding chemical cues for chemical communication along with the evolution of differentiated castes and increasingly larger, more complex colonies. The noneusocial German cockroach, on the other hand, seems to have conserved or even further expanded its repertoire of IRs, possibly allowing a better detection of a broad array of food sources and toxins, thus improving its survival chances in a an extremely challenging environment (Harrison, Arning et al., ).…”