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Minimal fermentative metabolism fuels extracellular symbiont in a leaf beetle.

ABSTRACT: While genome erosion is extensively studied in intracellular symbionts, the metabolic implications of reductive evolution in microbes subsisting extracellularly remain poorly understood. Stammera capleta-an extracellular symbiont in leaf beetles-possesses an extremely reduced genome (0.27?Mb), enabling the study of drastic reductive evolution in the absence of intracellularity. Here, we outline the genomic and transcriptomic profiles of Stammera and its host to elucidate host-symbiont metabolic interactions. Given the symbiont's substantial demands for nutrients and membrane components, the host's symbiotic organ shows repurposing of internal resources by upregulating nutrient transporters and cuticle-processing genes targeting epithelial chitin. Facilitated by this supplementation and its localization, Stammera exhibits a highly streamlined gene expression profile and a fermentation pathway for energy conversion, sharply contrasting the respiratory metabolism retained by most intracellular symbionts. Our results provide insights into a tightly regulated and metabolically integrated extracellular symbiosis, expanding our understanding of the minimal metabolism required to sustain life outside of a host cell.

SUBMITTER: Bauer E

PROVIDER: S-EPMC7031334 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Minimal fermentative metabolism fuels extracellular symbiont in a leaf beetle.

Bauer Eugen E Kaltenpoth Martin M Salem Hassan H

The ISME journal 20191203 3

While genome erosion is extensively studied in intracellular symbionts, the metabolic implications of reductive evolution in microbes subsisting extracellularly remain poorly understood. Stammera capleta-an extracellular symbiont in leaf beetles-possesses an extremely reduced genome (0.27 Mb), enabling the study of drastic reductive evolution in the absence of intracellularity. Here, we outline the genomic and transcriptomic profiles of Stammera and its host to elucidate host-symbiont metabolic ...[more]

PMID: 31796934

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Project description: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.

Dataset Information

Minimal fermentative metabolism fuels extracellular symbiont in a leaf beetle.

Publications

Minimal fermentative metabolism fuels extracellular symbiont in a leaf beetle.

Similar Datasets

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