Abstract

Measureable rates of genome evolution are well documented in human pathogens but are less well understood in bacterial pathogens in the wild, particularly during and after host switches. Mycoplasma gallisepticum (MG) is a pathogenic bacterium that has evolved predominantly in poultry and recently jumped to wild house finches (Carpodacus mexicanus), a common North American songbird. For the first time we characterize the genome and measure rates of genome evolution in House Finch isolates of MG, as well as in poultry outgroups. Using whole-genome sequences of 12 House Finch isolates across a 13-year serial sample and an additional four newly sequenced poultry strains, we estimate a nucleotide diversity in House Finch isolates of only ∼2% of ancestral poultry strains and a nucleotide substitution rate of 0.8−1.2×10−5 per site per year both in poultry and in House Finches, an exceptionally fast rate rivaling some of the highest estimates reported thus far for bacteria. We also found high diversity and complete turnover of CRISPR arrays in poultry MG strains prior to the switch to the House Finch host, but after the invasion of House Finches there is progressive loss of CRISPR repeat diversity, and recruitment of novel CRISPR repeats ceases. Recent (2007) House Finch MG strains retain only ∼50% of the CRISPR repertoire founding (1994–95) strains and have lost the CRISPR–associated genes required for CRISPR function. Our results suggest that genome evolution in bacterial pathogens of wild birds can be extremely rapid and in this case is accompanied by apparent functional loss of CRISPRs.

Highlights

  • Populations of animals are under constant threat from bacterial pathogens, which can be destructive following a switch to a new host or the evolution of novel virulence mechanisms

  • Around 1994, biologists noticed that House Finches were contracting conjunctivitis and Mycoplasma gallisepticum (MG) from poultry was discovered to be the cause

  • We sequenced the genomes of 12 House Finch MG strains sampled throughout the epizootic, from 1994–2007, as well as four additional putatively ancestral poultry MG strains

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Summary

Introduction

Populations of animals are under constant threat from bacterial pathogens, which can be destructive following a switch to a new host or the evolution of novel virulence mechanisms. In 1994, a strain of Mycoplasma gallisepticum (MG) was identified as the causative agent of an emerging epizootic in House Finches, a wild songbird inhabiting Eastern North America [1]. This bacterial pathogen frequently causes disease in commercial chicken and turkey flocks, but it had never been reported in House Finches or any songbird, leading to the suggestion that the epidemic began when MG expanded its host range from poultry to this phylogenetically distant songbird. The early detection of the epizootic allowed research and citizen-science teams to track its rapid spread throughout eastern North America in exceptional detail, making it one of the best documented wildlife pathogen outbreaks [3,4,5,6,7]

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