Interkingdom Gut Microbiome and Resistome of the Cockroach Blattella germanica

Abstract

Cockroaches are intriguing animals with two coexisting symbiotic systems, an endosymbiont in the fat body, involved in nitrogen metabolism, and a gut microbiome whose diversity, complexity, role, and developmental dynamics have not been fully elucidated. In this work, we present a metagenomic approach to study Blattella germanica populations not treated, treated with kanamycin, and recovered after treatment, both naturally and by adding feces to the diet, with the aim of better understanding the structure and function of its gut microbiome along the development as well as the characterization of its resistome. IMPORTANCE For the first time, we analyze the interkingdom hindgut microbiome of this species, including bacteria, fungi, archaea, and viruses. Network analysis reveals putative cooperation between core bacteria that could be key for ecosystem equilibrium. We also show how antibiotic treatments alter microbiota diversity and function, while both features are restored after one untreated generation. Combining data from B. germanica treated with three antibiotics, we have characterized this species’ resistome. It includes genes involved in resistance to several broad-spectrum antibiotics frequently used in the clinic. The presence of genetic elements involved in DNA mobilization indicates that they can be transferred among microbiota partners. Therefore, cockroaches can be considered reservoirs of antibiotic resistance genes (ARGs) and potential transmission vectors.

Gut Microbiota Cannot Compensate the Impact of (quasi) Aposymbiosis in Blattella germanica

“…The taxonomic distribution was analysed at the phylum level (Figure 4). The most abundant phyla in all the samples correspond to Bacteroidota, Firmicutes, Desulfobacterota (previously included in the phylum Proteobacteria [19]), Proteobacteria, Fusobacteriota, and Planctomycetota, as previously reported [7]. A strong reduction in Fusobacteria was observed in most treated samples in G2 and G3, and it was the only bacterial genus that was not recovered when no antibiotic was added in the following generations (unnoticeable amounts in all the samples from population RsCC, and three out of four samples of population RfCC).…”

“…In our previous work, we determined the putative functions of the gut microbiota, following a metagenomic approach [6,7]. However, the impact that those bacterial functions have on the host, and if they can somehow replace the endosymbiont's essential functions, have not been proven.…”

“…It was designed this way because the antibiotic treatment also affects the gut community and could reduce insect viability, and the treatment must be maintained during several generations, in order to progressively reduce the endosymbiont load. In fact, the microbiota's recovery is mainly expected by coprophagia once the antibiotic is removed [5][6][7], for which we expect there to be enough time because the females are dissected at least 20 days after the end of the treatment, i.e., the time necessary for the ootheca to hatch.…”

“…Such changes could be explained by a dependence on the presence/absence of competitors during hindgut colonization [20]. Previous studies on B. germanica revealed a complex gut community with an interdependent structure, which can be highly affected by antibiotic treatments, but it is also very robust and recovers after antibiotic exposure [5][6][7]. All those studies used longer treatment periods, even during full generations.…”

“…Later on, we tested the effect of different antibiotics (rifampicin [5], vancomycin and ampicillin [6], and kanamycin [7]) on the gut microbiota. In all four cases, a strong effect was observed on the treated generation, in terms of composition, diversity, and network complexity; however, only rifampicin reduced the Blattabacterium population [5], and its effect on the endosymbiont was observed in the following generation.…”