Comparative Whole-Genome Phylogeny of Animal, Environmental, and Human Strains Confirms the Genogroup Organization and Diversity of the Stenotrophomonas maltophilia Complex

Abstract

The Stenotrophomonas maltophilia complex (Smc) comprises opportunistic environmental Gram-negative bacilli responsible for a variety of infections in both humans and animals. Beyond its large genetic diversity, its genetic organization in genogroups was recently confirmed through the whole-genome sequencing of human and environmental strains. As they are poorly represented in these analyses, we sequenced the whole genomes of 93 animal strains to determine their genetic background and characteristics. Combining these data with 81 newly sequenced human strains and the genomes available from RefSeq, we performed a genomic analysis that included 375 nonduplicated genomes with various origins (animal, 104; human, 226; environment, 30; unknown, 15). Phylogenetic analysis and clustering based on genome-wide average nucleotide identity confirmed and specified the genetic organization of Smc in at least 20 genogroups. Two new genogroups were identified, and two previously described groups were further divided into two subgroups each. Comparing the strains isolated from different host types and their genogroup affiliation, we observed a clear disequilibrium in certain groups. Surprisingly, some antimicrobial resistance genes, integrons, and/or clusters of attC sites lacking integron-integrase (CALIN) sequences targeting antimicrobial compounds extensively used in animals were mainly identified in animal strains. We also identified genes commonly found in animal strains coding for efflux systems. The result of a large whole-genome analysis performed by us supports the hypothesis of the putative contribution of animals as a reservoir of Stenotrophomonas maltophilia complex strains and/or resistance genes for strains in humans. IMPORTANCE Given its naturally large antimicrobial resistance profile, the Stenotrophomonas maltophilia complex (Smc) is a set of emerging pathogens of immunosuppressed and cystic fibrosis patients. As it is group of environmental microorganisms, this adaptation to humans is an opportunity to understand the genetic and metabolic selective mechanisms involved in this process. The previously reported genomic organization was incomplete, as data from animal strains were underrepresented. We added the missing piece of the puzzle with whole-genome sequencing of 93 strains of animal origin. Beyond describing the phylogenetic organization, we confirmed the genetic diversity of the Smc, which could not be estimated through routine phenotype- or matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF)-based laboratory tests. Animals strains seem to play a key role in the diversity of Smc and could act as a reservoir for mobile resistance genes. Some genogroups seem to be associated with particular hosts; the genetic support of this association and the role of the determinants/corresponding genes need to be explored.

Genetic Variants of the DSF Quorum Sensing System in Stenotrophomonas maltophilia Influence Virulence and Resistance Phenotypes Among Genotypically Diverse Clinical Isolates

“…The other genogroups with a significant number of isolates in our collection were #2 (19%), #3 (13%) and C (15%), which is in agreement with the frequency of isolates belonging to these groups in the worldwide population. In agreement with previous studies (Corlouer et al, 2017;Mercier-Darty et al, 2020), genogroup #2 represents the most genetically diverse group in our collection. As proposed by Gröschel et al (2020) and shown in Supplementary Table S1, the strains could be further classified into the monophyletic lineages named Sm1-Sm18 (termed S. maltophilia sensu lato) or the more distantly related lineages Sgn1-Sgn4 according to Vinuesa et al (2018).…”

“…Due to these large genetic divergences, and because previously proposed species are recognized to be closely related to S. maltophilia, it is increasingly accepted to present it as the S. maltophilia complex (Svensson-Stadler et al, 2012;Patil et al, 2018;Vinuesa et al, 2018). PCRbased multilocus sequence typing (MLST) and whole-genome sequencing (WGS) have clearly shown the existence of several genomic or phylogenetic groups in the S. maltophilia complex, and have helped to clarify the taxonomic status of the species (Hauben et al, 1999;Kaiser et al, 2009;Ochoa-Sánchez and Vinuesa, 2017;Steinmann et al, 2018;Gröschel et al, 2020;Mercier-Darty et al, 2020). Even strains isolated from the same patient (Pompilio et al, 2016;Chung et al, 2017) or patients within the same hospital (Valdezate et al, 2004) can belong to distant phylogenetic groups with different phenotypes, probably due to the emergence of adaptive mutations as a result of selective pressure in the clinical environment or inside the host.…”

Multiple endogenous seed-born bacteria recovered rice growth disruption caused by Burkholderia glumae

“…Many S. maltophilia described that are responsible for a variety of infections in both humans and animals. By the comparative whole genome analysis of 375 unique S. maltophilia from various origins such as humans, other animals, and the environment, it was determined that bacteria originating from environment were distinct from those isolated from humans or other animals 38 . This indicates that RSB2 is unlikely to gain pathogenicity towards humans or other animals.…”

Modulated Response of Aspergillus fumigatus and Stenotrophomonas maltophilia to Antimicrobial Agents in Polymicrobial Biofilm

“…The genomic phylogeny of Sm was recently updated (Vinuesa et al, 2018 ) and S. maltophilia complex was defined, including Sm sensu stricto and several related genospecies. SM_CF is S. maltophilia sensu stricto through whole genome sequencing and phylogenomic analysis (Mercier-Darty et al, 2020 ). Both SM_REF and SM_CF belong to genogroup 6 (Hauben et al, 1999 ; Mercier-Darty et al, 2020 ), and no major difference in resistance genes was found.…”

“…SM_CF is S. maltophilia sensu stricto through whole genome sequencing and phylogenomic analysis (Mercier-Darty et al, 2020 ). Both SM_REF and SM_CF belong to genogroup 6 (Hauben et al, 1999 ; Mercier-Darty et al, 2020 ), and no major difference in resistance genes was found. Af strains were cultured on 2% malt agar containing 0.05% chloramphenicol at 37°C for 5 days.…”