Microbial Genomics - Online First

Bacteria and archaea make up most of natural diversity, but the mechanisms that underlie the origin and maintenance of prokaryotic species are poorly understood. We investigated the speciation history of the genus Salmonella , an ecologically diverse bacterial lineage, within which S. enterica subsp. enterica is responsible for important human food-borne infections. We performed a survey of diversity across a large reference collection using multilocus sequence typing, followed by genome sequencing of distinct lineages. We identified 11 distinct phylogroups, 3 of which were previously undescribed. Strains assigned to S. enterica subsp. salamae are polyphyletic, with two distinct lineages that we designate Salamae A and B. Strains of the subspecies houtenae are subdivided into two groups, Houtenae A and B, and are both related to Selander’s group VII. A phylogroup we designate VIII was previously unknown. A simple binary fission model of speciation cannot explain observed patterns of sequence diversity. In the recent past, there have been large-scale hybridization events involving an unsampled ancestral lineage and three distantly related lineages of the genus that have given rise to Houtenae A, Houtenae B and VII. We found no evidence for ongoing hybridization in the other eight lineages, but detected subtler signals of ancient recombination events. We are unable to fully resolve the speciation history of the genus, which might have involved additional speciation-by-hybridization or multi-way speciation events. Our results imply that traditional models of speciation by binary fission and divergence are not sufficient to account for Salmonella evolution.

Natural products (NPs), or specialized metabolites, are important for medicine and agriculture alike, and for the fitness of the organisms that produce them. NP genome-mining aims at extracting biosynthetic information from the genomes of microbes presumed to produce these compounds. Typically, canonical enzyme sequences from known biosynthetic systems are identified after sequence similarity searches. Despite this being an efficient process, the likelihood of identifying truly novel systems by this approach is low. To overcome this limitation, we previously introduced EvoMining, a genome-mining approach that incorporates evolutionary principles. Here, we release and use our latest EvoMining version, which includes novel visualization features and customizable databases, to analyse 42 central metabolic enzyme families (EFs) conserved throughout Actinobacteria , Cyanobacteria , Pseudomonas and Archaea. We found that expansion-and-recruitment profiles of these 42 families are lineage specific, opening the metabolic space related to ‘shell’ enzymes. These enzymes, which have been overlooked, are EFs with orthologues present in most of the genomes of a taxonomic group, but not in all. As a case study of canonical shell enzymes, we characterized the expansion and recruitment of glutamate dehydrogenase and acetolactate synthase into scytonemin biosynthesis, and into other central metabolic pathways driving Archaea and Bacteria adaptive evolution. By defining the origin and fate of enzymes, EvoMining complements traditional genome-mining approaches as an unbiased strategy and opens the door to gaining insights into the evolution of NP biosynthesis. We anticipate that EvoMining will be broadly used for evolutionary studies, and for generating predictions of unprecedented chemical scaffolds and new antibiotics. This article contains data hosted by Microreact.

Sequence type (ST)73 has emerged as one of the most frequently isolated extraintestinal pathogenic Escherichia coli. To examine the localized diversity of ST73 clonal groups, including their mobile genetic element profile, we sequenced the genomes of 16 multiple-drug resistant ST73 isolates from patients with urinary tract infection from a single hospital in Sydney, Australia, between 2009 and 2011. Genome sequences were used to generate a SNP-based phylogenetic tree to determine the relationship of these isolates in a global context with ST73 sequences (n=210) from public databases. There was no evidence of a dominant outbreak strain of ST73 in patients from this hospital, rather we identified at least eight separate groups, several of which reoccurred, over a 2 year period. The inferred phylogeny of all ST73 strains (n=226) including the ST73 clone D i2 reference genome shows high bootstrap support and clusters into four major groups that correlate with serotype. The Sydney ST73 strains carry a wide variety of virulence-associated genes, but the presence of iss, pic and several iron-acquisition operons was notable.