Incipient genome erosion and metabolic streamlining for antibiotic production in a defensive symbiont

Nechitaylo, Taras Y. and Sandoval-Calderon, Mario and Engl, Tobias and Wielsch, Natalie and Dunn, Diane M. and Goesmann, Alexander and Strohm, Erhard and Svatos, Ales and Dale, Colin and Weiss, Robert B. and Kaltenpoth, Martin (2021) Incipient genome erosion and metabolic streamlining for antibiotic production in a defensive symbiont. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 118 (17): e202304711. ISSN 0027-8424, 1091-6490

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Abstract

Genome erosion is a frequently observed result of relaxed selection in insect nutritional symbionts, but it has rarely been studied in defensive mutualisms. Solitary beewolf wasps harbor an actinobacterial symbiont of the genus Streptomyces that provides protection to the developing offspring against pathogenic microorganisms. Here, we characterized the genomic architecture and functional gene content of this culturable symbiont using genomics, transcriptomics, and proteomics in combination with in vitro assays. Despite retaining a large linear chromosome (7.3 Mb), the wasp symbiont accumulated frameshift mutations in more than a third of its protein-coding genes, indicative of incipient genome erosion. Although many of the frameshifted genes were still expressed, the encoded proteins were not detected, indicating post-transcriptional regulation. Most pseudogenization events affected accessory genes, regulators, and transporters, but "Streptomyces philanthi" also experienced mutations in central metabolic pathways, resulting in auxotrophies for biotin, proline, and arginine that were confirmed experimentally in axenic culture. In contrast to the strong A+T bias in the genomes of most obligate symbionts, we observed a significant G+C enrichment in regions likely experiencing reduced selection. Differential expression analyses revealed that-compared to in vitro symbiont cultures-"S. philanthi" in beewolf antennae showed overexpression of genes for antibiotic biosynthesis, the uptake of host-provided nutrients and the metabolism of building blocks required for antibiotic production. Our results show unusual traits in the early stage of genome erosion in a defensive symbiont and suggest tight integration of host-symbiont metabolic pathways that effectively grants the host control over the antimicrobial activity of its bacterial partner.

Item Type: Article
Uncontrolled Keywords: BACTERIAL ENDOSYMBIONT; STREPTOMYCES-PHILANTHI; PROKARYOTIC GENOMES; EVOLUTION; SEQUENCE; PROTECT; GROEL; RECONSTRUCTION; TRANSCRIPTOME; HYMENOPTERA; defensive symbiosis; protective mutualism; genome erosion; pseudogenization; Streptomyces
Subjects: 500 Science > 590 Zoological sciences
Divisions: Biology, Preclinical Medicine > Institut für Zoologie > Evolutionary Ecology (Prof. Dr. Erhard Strohm)
Depositing User: Dr. Gernot Deinzer
Date Deposited: 16 Sep 2022 11:42
Last Modified: 16 Sep 2022 11:42
URI: https://pred.uni-regensburg.de/id/eprint/47549

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