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Symbiont Genomic Features and Localization in the Bean Beetle Callosobruchus maculatus.

ABSTRACT: A pervasive pest of stored leguminous products, the bean beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae) associates with a simple bacterial community during adulthood. Despite its economic importance, little is known about the compositional stability, heritability, localization, and metabolic potential of the bacterial symbionts of C. maculatus. In this study, we applied community profiling using 16S rRNA gene sequencing to reveal a highly conserved bacterial assembly shared between larvae and adults. Dominated by Firmicutes and Proteobacteria, this community is localized extracellularly along the epithelial lining of the bean beetle's digestive tract. Our analysis revealed that only one species, Staphylococcus gallinarum (phylum Firmicutes), is shared across all developmental stages. Isolation and whole-genome sequencing of S. gallinarum from the beetle gut yielded a circular chromosome (2.8 Mb) and one plasmid (45 kb). The strain encodes complete biosynthetic pathways for the production of B vitamins and amino acids, including tyrosine, which is increasingly recognized as an important symbiont-supplemented precursor for cuticle biosynthesis in beetles. A carbohydrate-active enzyme search revealed that the genome codes for a number of digestive enzymes, reflecting the nutritional ecology of C. maculatus. The ontogenic conservation of the gut microbiota in the bean beetle, featuring a "core" community composed of S. gallinarum, may be indicative of an adaptive role for the host. In clarifying symbiont localization and metabolic potential, we further our understanding and study of a costly pest of stored products. IMPORTANCE From supplementing essential nutrients to detoxifying plant secondary metabolites and insecticides, bacterial symbionts are a key source of adaptations for herbivorous insect pests. Despite the pervasiveness and geographical range of the bean beetle Callosobruchus maculatus, the role of microbial symbioses in its natural history remains understudied. Here, we demonstrate that the bean beetle harbors a simple gut bacterial community that is stable throughout development. This community localizes along the insect's digestive tract and is largely dominated by Staphylococcus gallinarum. In elucidating symbiont metabolic potential, we highlight its possible adaptive significance for a widespread agricultural pest.

SUBMITTER: Berasategui A

PROVIDER: S-EPMC8174668 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe thermal plasticity of life-history traits receives wide attention in the recent biological literature. Of all the temperature-dependent traits studied, developmental rates of ectotherms are especially often addressed, and yet surprisingly little is known about embryonic responses to temperature, including changes in the thermal thresholds and thermal sensitivity during early development. Even postembryonic development of many cryptically living species is understood superficially at best.ResultsThis study is the first to estimate the exact durations of developmental stages in the cowpea seed beetle C. maculatus from oviposition to adult emergence at five permissive constant temperatures from 20 to 32 °C. Early embryonic development was tracked and documented by means of destructive sampling and subsequent confocal imaging of fluorescently stained specimens. Late embryonic and early larval development was studied with the use of destructive sampling and light microscopy. Well-resolved temporal series based on thousands of embryos allowed precise timing of the following developmental events: formation of the blastoderm; formation, elongation, and retraction of the germ band; dorsal closure; the onset and completion of sclerotization of the cuticle; hatching, and penetration of the first-instar larva into the cowpea seed. Pupation and adult eclosion were observed directly through an incision in the seed coat. The thermal phenotype of C. maculatus was found to vary in the course of ontogeny and different stages scaled disproportionately with temperature, but pitfalls and caveats associated with analyses of relative durations of individual stages are also briefly discussed.ConclusionDisproportionate changes in developmental durations with temperature may have important implications when study design requires a high degree of synchronization among experimental embryos or when the occurrence of particular stages in the field is of interest, as well as in any other cases when development times need to be estimated with precision. This work provides one of the first examples of integration of embryological techniques with ecophysiological concepts and will hopefully motivate similar projects in the future. While experiments with Drosophila continue to be the main source of information on animal development, knowledge on other model species is instrumental to building a broader picture of developmental phenomena.

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Symbiont Genomic Features and Localization in the Bean Beetle Callosobruchus maculatus.

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