Population Gene Introgression and High Genome Plasticity for the Zoonotic Pathogen Streptococcus agalactiae

Abstract

The influence that bacterial adaptation (or niche partitioning) within species has on gene spillover and transmission among bacterial populations occupying different niches is not well understood. Streptococcus agalactiae is an important bacterial pathogen that has a taxonomically diverse host range making it an excellent model system to study these processes. Here, we analyze a global set of 901 genome sequences from nine diverse host species to advance our understanding of these processes. Bayesian clustering analysis delineated 12 major populations that closely aligned with niches. Comparative genomics revealed extensive gene gain/loss among populations and a large pan genome of 9,527 genes, which remained open and was strongly partitioned among niches. As a result, the biochemical characteristics of 11 populations were highly distinctive (significantly enriched). Positive selection was detected and biochemical characteristics of the dispensable genes under selection were enriched in ten populations. Despite the strong gene partitioning, phylogenomics detected gene spillover. In particular, tetracycline resistance (which likely evolved in the human-associated population) from humans to bovine, canines, seals, and fish, demonstrating how a gene selected in one host can ultimately be transmitted into another, and biased transmission from humans to bovines was confirmed with a Bayesian migration analysis. Our findings show high bacterial genome plasticity acting in balance with selection pressure from distinct functional requirements of niches that is associated with an extensive and highly partitioned dispensable genome, likely facilitating continued and expansive adaptation.

Development and Application of a Prophage Integrase Typing Scheme for Group B Streptococcus

“…Based on integrase typing, false positive results may also occur, as demonstrated for GBS Int 5, which was found once as part of a full prophage (isolate QMA0323, piscine ST261; Kawasaki et al, 2018 ) and once as a singleton within a larger ICE (isolate FSL S3-026, bovine ST67; Richards et al, 2011 ). A BLAST search of genomes with more than 50 contigs showed the presence of GBS Int 5 as a singleton within an ICE rather than as part of a full prophage in nine bovine GBS genomes from bovine-associated lineage CC67 (Richards et al, 2019 ). This phenomenon was only observed for GBS Int 5, possibly because its insertion site, rpsI (30S ribosomal protein S9), is a hotspot for recombination of ICE in streptococcal species (Brochet et al, 2008 ; Ambroset et al, 2016 ).…”

“…To make the prophage and integrase database more comprehensive, a second dataset (dataset 2, Table S2 ) was subsequently screened, consisting of genomes that were of high quality, albeit not necessarily closed, and providing more in-depth coverage of major and minor GBS host species, geographic diversity, and GBS clades. Dataset 2 is a subset of 901 publicly available sequences included in the study by Richards et al ( 2019 ) and includes all sequences with a maximum of 50 contigs ( n = 503). Isolates with more than 50 contigs were excluded from analysis because high genome fragmentation can lead to sub-optimal performance of bioinformatic programs.…”

“…Group B Streptococcus (GBS)—also known as Streptococcus agalactiae —is a gram-positive bacterium with a wide host range (Brochet et al, 2006 ; Delannoy et al, 2016 ; Richards et al, 2019 ). Major hosts of interest from a public health and socio-economic point of view are humans (High et al, 2005 ; Le Doare et al, 2017 ; Seale et al, 2017 ), fishes (Jafar et al, 2008 ; Liu et al, 2014 ; Zamri-Saad, 2018 ), and cattle (Zadoks et al, 2011 ; Lyhs et al, 2016 ; Sørensen et al, 2019 ).…”

“…The epidemiology and clinical manifestations of GBS disease in humans continue to evolve, as exemplified by the recent emergence of hypervirulent GBS in adults without underlying comorbidities (Barkham et al, 2019 ). Phages and other mobile genetic elements (MGE) play an important role in the evolution of GBS, its adaptation to different hosts and niches and its virulence profile (Richards et al, 2019 ). In human isolates, a high prevalence of prophages has been associated with greater pathogenicity, particularly the ability to cause invasive infections (van der Mee-Marquet et al, 2006 ; Domelier et al, 2009 ; Salloum et al, 2010 , 2011 ).…”

The fall and rise of group BStreptococcusin dairy cattle: reintroduction due to human-to-cattle host jumps?

“…Emergence of GBS in animal production systems occurred concurrently with changes in husbandry practices, such as use of milking machines, or the intensification of commercial aquaculture [3,8,9].…”