Molecular causes of an evolutionary shift along the parasitism-mutualism continuum in a bacterial symbiont

Author(s)
Paul Herrera, Lisa Schuster, Cecilia Wentrup, Lena König, Thomas Kempinger, Hyunsoo Na, Jasmin Schwarz, Stephan Köstlbacher, Florian Wascher, Markus Zojer, Thomas Rattei, Matthias Horn
Abstract

Symbiosis with microbes is a ubiquitous phenomenon with a massive impact on all living organisms, shaping the world around us today. Theoretical and experimental studies show that vertical transmission of symbionts leads to the evolution of mutualistic traits, whereas horizontal transmission facilitates the emergence of parasitic features. However, these studies focused on phenotypic data, and we know little about underlying molecular changes at the genomic level. Here, we combined an experimental evolution approach with infection assays, genome resequencing, and global gene expression analysis to study the effect of transmission mode on an obligate intracellular bacterial symbiont. We show that a dramatic shift in the frequency of genetic variants, coupled with major changes in gene expression, allow the symbiont to alter its position in the parasitism-mutualism continuum depending on the mode of between-host transmission. We found that increased parasitism in horizontally transmitted chlamydiae residing in amoebae was a result of processes occurring at the infectious stage of the symbiont's developmental cycle. Specifically, genes involved in energy production required for extracellular survival and the type III secretion system-the symbiont's primary virulence mechanism-were significantly up-regulated. Our results identify the genomic and transcriptional dynamics sufficient to favor parasitic or mutualistic strategies.

Organisation(s)
Centre for Microbiology and Environmental Systems Science, Department of Microbiology and Ecosystem Science
Journal
Proceedings of the National Academy of Sciences of the United States of America (PNAS)
Volume
117
Pages
21658-21666
No. of pages
9
ISSN
0027-8424
DOI
https://doi.org/10.1073/pnas.2005536117
Publication date
08-2020
Peer reviewed
Yes
Austrian Fields of Science 2012
106005 Bioinformatics, 106022 Microbiology
Keywords
ASJC Scopus subject areas
General
Portal url
https://ucrisportal.univie.ac.at/en/publications/molecular-causes-of-an-evolutionary-shift-along-the-parasitismmutualism-continuum-in-a-bacterial-symbiont(4edaf5f0-beef-41f7-9f91-af40b2d188e5).html