Diversity and Composition of the Gut Microbiota in the Developmental Stages of the Dung Beetle Copris incertus Say (Coleoptera, Scarabaeidae)

Abstract

Dung beetles are holometabolous insects that feed on herbivorous mammal dung and provide services to the ecosystem including nutrient cycling and soil fertilization. It has been suggested that organisms developing on incomplete diets such as dungs require the association with microorganisms for the synthesis and utilization of nutrients. We describe the diversity and composition of the gut-microbiota during the life cycle of the dung beetle Copris incertus using 16S rRNA gene sequencing. We found that C. incertus gut contained a broad diversity of bacterial groups (1,699 OTUs and 302 genera). The taxonomic composition varied during the beetle life cycle, with the predominance of some bacterial genera in a specific developmental stage (Mothers: Enterobacter and Serratia; Eggs: Nocardioides and Hydrogenophaga; Larval and pupal stages: Dysgonomonas and Parabacteroides; offspring: Ochrobactrum). The beta diversity evidenced similarities among developmental stages, clustering (i) the adult stages (mother, male and female offsprings), (ii) intermediate developmental (larvae and pupa), and (iii) initial stage (egg). Microbiota differences could be attributed to dietary specialization or/and morpho-physiological factors involved in the transition from a developmental stage to the next. The predicted functional profile (PICRUSt2 analysis) for the development bacterial core of the level 3 categories, indicated grouping by developmental stage. Only 36 categories were significant in the SIMPER analysis, including the metabolic categories of amino acids and antibiotic synthesis, which were enriched in the larval and pupal stages; both categories are involved in the metamorphosis process. At the gene level, we found significant differences only in the KOs encoding functions related to nitrogen fixation, uric acid metabolism, and plant cell wall degradation for all developmental stages. Nitrogen fixation and plant cell wall degradation were enriched in the intermediate stages and uric acid metabolism was enriched in mothers. The data reported here suggested the influence of the maternal microbiota in the composition and diversity of the gut microbiota of the offspring.

Ontogeny, species identity, and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae)

“…Similar examples of decreasing microbiome diversity can be found throughout the lifecycle of some holometabolous insects, e.g., dung beetles [94] and cabbage flies [95]. For holometabolous insects, ontogenetic changes in gut bacterial communities are generally explained by two main factors: the substantial remodelling of the gastrointestinal tract during metamorphosis [89] and different dietary needs between larvae and adults [94]. Although hemimetabolous Triatominae depend on a blood-based diet throughout their entire development, their preferences for accessory feeding strategies, especially haemolymphagy and coprophagy, may decrease over time and thus limit opportunities for any microbiome enrichment.…”

“…However, the relationship between ontogeny and microbiome composition has not been investigated in other hemimetabolous bloodfeeding insects (bed bugs or lice [21];), making generalisable conclusions between biologically similar taxa elusive. Similar examples of decreasing microbiome diversity can be found throughout the lifecycle of some holometabolous insects, e.g., dung beetles [94] and cabbage flies [95]. For holometabolous insects, ontogenetic changes in gut bacterial communities are generally explained by two main factors: the substantial remodelling of the gastrointestinal tract during metamorphosis [89] and different dietary needs between larvae and adults [94].…”

The Role of Bacterial Symbionts in Triatomines: An Evolutionary Perspective

“…Holometabolous insects revert to an almost-axenic state during pupation and some of the microbiota is acquired anew by adults from the environment after emergence [ 8 , 14 , 15 , 62 , 63 , 64 , 65 ]. In some species, adults may harbor a very distinct microbiota than the immature stages [ 10 , 11 , 12 , 66 , 67 , 68 , 69 ] or acquire a very similar microbiota from the environment or conspecifics [ 13 , 70 , 71 ]. In contrast, in hemimetabolous insects, microbes that are acquired after hatching can be maintained for a lifetime [ 8 , 9 ].…”

“…Whereas nymphs of hemimetabolous insects may carry their microbiota from early nymphal stages through to the adult stages [ 8 , 9 ], the transformation from larva–pupa–adult in holometabolous insects involves the breakdown of the larval GI tract and the construction of the adult GI tract. During this metamorphosis, there is a high expression of antimicrobial compounds that eliminate most gut bacterial symbionts [ 8 , 10 , 11 ], and can lead to the establishment of a different microbiome in adults [ 12 ]. Adult holometabolous insect may need to reacquire most of their microbiota [ 11 , 13 , 14 ] or to develop strategies to avoid the elimination of existing microbes during molting [ 15 , 16 , 17 ].…”

“…During this metamorphosis, there is a high expression of antimicrobial compounds that eliminate most gut bacterial symbionts [ 8 , 10 , 11 ], and can lead to the establishment of a different microbiome in adults [ 12 ]. Adult holometabolous insect may need to reacquire most of their microbiota [ 11 , 13 , 14 ] or to develop strategies to avoid the elimination of existing microbes during molting [ 15 , 16 , 17 ].…”