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.
Highlights
Symbiosis with microbes is a ubiquitous phenomenon with a massive impact on all living organisms, shaping the world around us today
The relationship between the partners in microbial symbioses have been described as existing along a parasitism–mutualism continuum [1], and the dynamics of this continuum are dependent upon numerous genotypic and environmental factors [2,3,4,5,6]
The mode of symbiont transmission among host generations has important evolutionary ramifications: while vertical transmission (VT) aligns the evolutionary interest of host and symbionts, selecting for benign or even mutualistic symbionts, HT does not penalize parasitic strategies, because symbionts are associated with a new host individual every round [11,12,13,14]
Summary
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. These studies focused on phenotypic data, and we know little about underlying molecular changes at the genomic level. During host cell division this symbiont can be vertically transmitted from parent to daughter cells (VT), but can readily infect naive hosts (HT) This mixed transmission mode [29] represents an ideal starting point for experimentally manipulating the transmission of symbionts among host generations (i.e., VT or HT), and in this way identify the molecular changes that arise in response to the different selection regimes
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