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Ecological relevance and molecular regulation of antibiotic-producing bacterial symbionts in Lagriinae beetles

Applicant Professor Dr. Martin Kaltenpoth, since 4/2021
Subject Area Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Microbial Ecology and Applied Microbiology
Systematics and Morphology (Zoology)
Term from 2019 to 2022
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 416606594
 
Final Report Year 2023

Final Report Abstract

Symbiotic interactions with microorganisms are a driving force in the evolution of multicellular organisms. Along with nutritional symbioses, those with a defensive basis are frequent in nature, yet less is known about their ecology and evolution, especially under natural conditions. Lagriinae beetles engage in a symbiosis with multiple strains of Burkholderia gladioli bacteria, which are transmitted from mother to offspring and can protect the host eggs from antagonistic fungi. Recent findings show that co-existing symbiont strains can each produce a distinct set of bioactive secondary metabolites with antimicrobial activities. Using this model system, our aim was to better understand the ecology, evolution and molecular basis of defensive symbiosis. The first part of the project focused on the ecological relevance of symbiont-mediated defense during host development and across Lagriinae species. Using a combination of analytical chemistry, mass-spectrometry imaging, fluorescence insitu hybridization (FISH) and manipulative bioassays, we demonstrated that Burkholderia provide protection to the beetles that extends beyond the eggs stage and across larval and pupal development, shielding in particular the vulnerable post-molting phases of the larvae from fungal infections. Microscopy and micro-computed tomography revealed morphological adaptations for symbiont maintenance and translocation through metamorphosis, providing an explanation for how the symbiosis can be stably maintained over evolutionary timescales. A comparison of symbiont strain dynamics and function between two congeneric Lagria species uncovered functional similarity in both symbioses, but differences in prevalence and relative abundance of coexisting symbiont strains. In order to unravel the molecular factors underlying the establishment and maintenance of symbiosis, we genetically manipulated the culturable symbiont strain LvStA and used transposon-insertion sequencing as a genome-wide unbiased approach for identifying candidate genes essential for host colonization. This technique yielded 262 candidate colonization factors, including genes involved in flagellar motility, lipopeptide biosynthesis, stress response and iron metabolism. On the host side, transcriptome sequencing across developmental stages revealed an upregulation of immune-related genes in symbiotic vs. aposymbiotic beetles, suggesting an active cross-talk between the symbiotic partners. Our results contribute to the general understanding of animal-microbe interactions in the context of host protection and provide valuable insights on the evolution and stability of multi-strain symbiotic interactions.

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