Developmental stages and gut microenvironments influence gut microbiota dynamics in the invasive beetle Popillia japonica Newman (Coleoptera: Scarabaeidae)

Abstract

Summary Popillia japonica Newman (Coleoptera: Scarabaeidae) is a highly polyphagous invasive beetle originating from Japan. This insect is highly resilient and able to rapidly adapt to new vegetation. Insect‐associated microorganisms can play important roles in insect physiology, helping their hosts to adapt to changing conditions and potentially contributing to an insect's invasive potential. Such symbiotic bacteria can be part of a core microbiota that is stably transmitted throughout the host's life cycle or selectively recruited from the environment at each developmental stage. The aim of this study was to investigate the origin, stability and turnover of the bacterial communities associated with an invasive population of P. japonica from Italy. Our results demonstrate that soil microbes represent an important source of gut bacteria for P. japonica larvae, but as the insect develops, its gut microbiota richness and diversity decreased substantially, paralleled by changes in community composition. Notably, only 16.75% of the soil bacteria present in larvae are maintained until the adult stage. We further identified the micro‐environments of different gut sections as an important factor shaping microbiota composition in this species, likely due to differences in pH, oxygen availability and redox potential. In addition, P. japonica also harboured a stable bacterial community across all developmental stages, consisting of taxa well known for the degradation of plant material, namely the families Ruminococcacae, Christensenellaceae and Lachnospiraceae. Interestingly, the family Christensenallaceae had so far been observed exclusively in humans. However, the Christensenellaceae operational taxonomic units found in P. japonica belong to different taxonomic clades within this family.

Divergence in Gut Bacterial Community Among Life Stages of the Rainbow Stag Beetle Phalacrognathus muelleri (Coleptera: Lucanidae)

“…They were primarily involved in lignocellulose decomposition, food fermentation and enhancement of metabolic capacity of the host [ 4 , 62 , 63 ]. This information illustrated that different diets cause differences in gut bacteria, a result that has been reported in the scarab beetle, Popillia japonica [ 7 ], in the fruit fly Drosophila suzukiiis and in the pine weevil Hylobius abietis [ 52 , 64 ].…”

“…Four phyla—Firmicutes, Proteobacteria, Bacteroidetes and Tenericutes—were predominant in the gut bacteria across all stages, which is consistent with prior studies in other beetles (i.e., bark beetles, longhorn beetles, herbivorous beetles and burying beetles) [ 12 , 13 , 26 , 47 ]. Firmicutes and Proteobacteria were the dominant phyla in Anoplophora glabripennis [ 12 ], Hylobius abietis [ 48 ], Monochamus alternatus and Psacothea hilaris [ 4 ], Nicrophorus vespilloides [ 26 ], and Popillia japonica [ 7 ]. Firmicutes, Proteobacteria and Bacteroidetes were also the dominant phyla in Holotrichia parallela [ 47 ], Dendroctonus valens [ 13 ], and Dendroctonus rhizophagus [ 10 ], and Tenericutes also was the dominant phylum in Odontolabis fallaciosa (Lucanidae) [ 34 ].…”

“…Almost all beetles undergo holometabolism, including a pupal stage compared with incomplete metamorphosis. The study of Agrilus mali (Coleoptera: Buprestidae) and Popillia japonica (Coleoptera: Scarabaeidae) has suggested that the metabolic activity of the intestine decreases in the pupal stage and morphology changes during the insects’ metamorphosis influence the associated bacteria communities [ 3 , 7 ]. Moreover, larvae and adults feed on different foods, thus, occupying distinct ecological niches in the carbon cycle of forest ecosystems [ 8 ].…”

Hydrolytic Profile of the Culturable Gut Bacterial Community Associated With Hermetia illucens

“…Taking into account its hydrolytic degradation abilities on complex substrates, BSF could be considered a potential source of enzymes with important industrial applications: recently polymer-degrading enzymes, such as cellulases and serine proteases, have been indeed characterized from H. illucens holobiont (Kim et al, 2011a;Lee et al, 2014). However, since strong variations of pH levels, ranging from slightly acidic conditions in the anterior part, to strong acidic values in the middle portion, and to alkaline values in the posterior region, have been reported in BSF midgut (Bonelli et al, 2019;Bruno et al, 2019) and also considering that hypoxic and anoxic conditions might occur in BSF gut (Engel and Moran, 2013;Chouaia et al, 2019), further quantitative verifications of the metabolic activities of the isolates (and of their combination) should be performed under different oxygen concentrations and pH levels, especially regarding the strain B. licheniformis HI169, which showed the best performances in in vivo tests.…”

Gut Bacteria in the Holometabola: A Review of Obligate and Facultative Symbionts

“…Further survey and functional assessment of symbionts in successful phytophagous beetle lineages that primarily harbor facultative gut bacteria including the Buprestidae ( Vasanthakumar et al 2008 , Bozorov et al 2019 ) and Cerambycidae ( Ayayee et al 2014 , Ayayee et al 2016 , Mohammed et al 2018 ) will be necessary to assess the evolution of dependence on obligate bacteria compared with facultatives. The widespread strategy of harboring cellulolytic bacteria in the Scarabaeoidea whose larvae feed primarily on living and dead plant tissue ( Egert et al 2003 , 2005 ; Arias-Cordero et al 2012 ; Ceja-Navarro et al 2014 ; Zhang et al 2018 ; Chouaia et al 2019 ) further emphasizes the need to look more precisely at host biology. Patterns based on general feeding guild do little to elucidate bacterial services beyond gross conjecture.…”