Patterns of genome evolution that have accompanied host adaptation in Salmonella

Abstract

Many bacterial pathogens are specialized, infecting one or few hosts, and this is often associated with more acute disease presentation. Specific genomes show markers of this specialization, which often reflect a balance between gene acquisition and functional gene loss. Within Salmonella enterica subspecies enterica, a single lineage exists that includes human and animal pathogens adapted to cause infection in different hosts, including S. enterica serovar Enteritidis (multiple hosts), S. Gallinarum (birds), and S. Dublin (cattle). This provides an excellent evolutionary context in which differences between these pathogen genomes can be related to host range. Genome sequences were obtained from ∼60 isolates selected to represent the known diversity of this lineage. Examination and comparison of the clades within the phylogeny of this lineage revealed signs of host restriction as well as evolutionary events that mark a path to host generalism. We have identified the nature and order of events for both evolutionary trajectories. The impact of functional gene loss was predicted based upon position within metabolic pathways and confirmed with phenotyping assays. The structure of S. Enteritidis is more complex than previously known, as a second clade of S. Enteritidis was revealed that is distinct from those commonly seen to cause disease in humans or animals, and that is more closely related to S. Gallinarum. Isolates from this second clade were tested in a chick model of infection and exhibited a reduced colonization phenotype, which we postulate represents an intermediate stage in pathogen-host adaptation.Salmonella | host adaptation | pseudogene | metabolism

The Periplasmic Nitrate Reductase NapABC Supports Luminal Growth of Salmonella enterica Serovar Typhimurium during Colitis

“…Comparison of the genomes of serovars belonging to the gastrointestinal pathovar with those belonging to the extraintestinal pathovar identifies genes important for intestinal survival, because they are undergoing decay in the latter group (43). That is, extraintestinal serovars accumulate mutations affecting genes important only for luminal growth, since no selective pressure exists to preserve their function; the result is pseudogene formation (43)(44)(45). Analysis of the nitrate reductases and their regulators found that only the narQP two-component system was rendered nonfunctional in extraintestinal serovars due to mutations (43).…”

Genomic Analysis of Salmonella enterica Serovar Typhimurium from Wild Passerines in England and Wales

“…However, long-read sequencing is necessary to identify the exact composition and orientation of the prophages in these isolates. While there are no individual genes that are present uniquely in every clade A isolate, it is also possible that pseudogenes or SNPs may be related to adaptation to specific hosts or a systemic rather than gastrointestinal infection lifestyle as has been identified previously (30,62,63). The loss of diverse metabolic pathways that allow persistence in the gastrointestinal tract of the chicken during experimental infection is a feature common to the galliform-adapted Salmonella enterica subsp.…”

Evolution of host specialization in gut microbes: the bee gut as a model

“…In Salmonella enterica, a widespread pathogen of mammals and birds, adaptation to hosts is thought to be multifactorial, with both gene gain and loss playing a part. 41,42 However, it is unclear whether these events are the cause or consequence of specialization. A recent gene-swapping study of V. fischeri strains hosted by Australian or Hawaiian Euprymna squids suggested that multifactor-mediated host specificity is not incompatible with single loci of large effect: there may in fact be multiple genes in a genome capable of greatly altering host affinity.…”

“…44,45 The horizontal acquisition of the permissive effector genes can lead to effective colonization of the same host plant by distantly related pathogen strains, thus breaking apart the phylogenetic hostmicrobe correlations typically associated with co-evolved symbioses. 44,45 Both horizontal gene transfer and genomic degradation probably play prominent roles in the evolution of specialization, 42,46 but to what extent remains an unresolved question. There is also the host perspective to consider, as interplay between host immunity and the microbiota constitutes an ongoing dialog between partners that often have competing evolutionary interests.…”