Intracellular symbiont Symbiodolus is vertically transmitted and widespread across insect orders.

Insect Symbiosis intracellular secretion system symbiont vertical transmission

Journal

The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086

Informations de publication

Date de publication:
14 Jun 2024
Historique:
received: 06 02 2024
revised: 05 04 2024
medline: 14 6 2024
pubmed: 14 6 2024
entrez: 14 6 2024
Statut: aheadofprint

Résumé

Insects engage in manifold interactions with bacteria that can shift along the parasitism-mutualism continuum. However, only a small number of bacterial taxa managed to successfully colonize a wide diversity of insects, by evolving mechanisms for host-cell entry, immune evasion, germline tropism, reproductive manipulation, and/or by providing benefits to the host that stabilize the symbiotic association. Here we report on the discovery of an Enterobacterales endosymbiont (Symbiodolus, type species S. clandestinus) that is widespread across at least six insect orders and occurs at high prevalence within host populations. Fluorescence in situ hybridization in several Coleopteran and one Dipteran species revealed Symbiodolus' intracellular presence in all host life stages and across tissues, with a high abundance in female ovaries, indicating transovarial vertical transmission. Symbiont genome sequencing across 16 host taxa revealed a high degree of functional conservation in the eroding and transposon-rich genomes. All sequenced Symbiodolus genomes encode for multiple secretion systems, alongside effectors and toxin-antitoxin systems, which likely facilitate host-cell entry and interactions with the host. However, Symbiodolus-infected insects show no obvious signs of disease, and biosynthetic pathways for several amino acids and cofactors encoded by the bacterial genomes suggest that the symbionts may also be able to provide benefits to the hosts. A lack of host-symbiont cospeciation provides evidence for occasional horizontal transmission, so Symbiodolus' success is likely based on a mixed transmission mode. Our findings uncover a hitherto undescribed and widespread insect endosymbiont that may present valuable opportunities to unravel the molecular underpinnings of symbiosis establishment and maintenance.

Identifiants

pubmed: 38874172
pii: 7693286
doi: 10.1093/ismejo/wrae099
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) [2024]. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.

Auteurs

Jürgen C Wierz (JC)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

Philipp Dirksen (P)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.
Department of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg University, Mainz, Germany.

Roy Kirsch (R)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

Ronja Krüsemer (R)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

Benjamin Weiss (B)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

Yannick Pauchet (Y)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

Tobias Engl (T)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

Martin Kaltenpoth (M)

Department of Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany.

Classifications MeSH