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The Versatility of Opportunistic Infections Caused by Gemella Isolates Is Supported by the Carriage of Virulence Factors from Multiple Origins

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The Versatility of Opportunistic Infections Caused by Gemella Isolates Is Supported by the Carriage of Virulence Factors from Multiple Origins fmicb-11-00524 March 27, 2020 Time: 17:39 # 1 ORIGINAL RESEARCH published: 31 March 2020 doi: 10.3389/fmicb.2020.00524 The Versatility of Opportunistic Infections Caused by Gemella Isolates Is Supported by the Carriage of Virulence Factors From Multiple Origins Ernesto García López1,2 and Antonio J. Martín-Galiano3* 1 Departamento de Biotecnología Microbiana y de Plantas, Centro de Investigaciones Biológicas (CSIC), Madrid, Spain, 2 CIBER de Enfermedades Respiratorias (CIBERES), Madrid, Spain, 3 Intrahospital Infections Laboratory, National Centre for Microbiology, Instituto de Salud Carlos III (ISCIII), Majadahonda, Spain The molecular basis of the pathogenesis of the opportunistic invasive infections caused by isolates of the Gemella genus remains largely unknown. Moreover, inconsistencies Edited by: in the current species assignation were detected after genome-level comparison of Lisa Sedger, University of Technology Sydney, 16 public Gemella isolates. A literature search detected that, between the two most Australia pathogenic species, Gemella morbillorum causes about twice the number of cases Reviewed by: compared to Gemella haemolysans. These two species shared their mean diseases – Erik Senneby, Lund University, Sweden sepsis and endocarditis – but differed in causing other syndromes. A number of Rosalia Cavaliere, well-known virulence factors were harbored by all species, such as a manganese University of Technology Sydney, transport/adhesin sharing 83% identity from oral endocarditis-causing streptococci. Australia Likewise, all Gemellae carried the genes required for incorporating phosphorylcholine *Correspondence: Antonio J. Martín-Galiano into their cell walls and encoded some choline-binding proteins. In contrast, other [email protected] proteins were species-specific, which may justify the known epidemiological differences. G. haemolysans, but not G. morbillorum, harbor a gene cluster potentially encoding a Specialty section: This article was submitted to polysaccharidic capsule. Species-specific surface determinants also included Rib and Infectious Diseases, MucBP repeats, hemoglobin-binding NEAT domains, peptidases of C5a complement a section of the journal Frontiers in Microbiology factor and domains that recognize extracellular matrix molecules exposed in damaged Received: 05 November 2019 heart valves, such as collagen and fibronectin. Surface virulence determinants were Accepted: 11 March 2020 associated with several taxonomically dispersed opportunistic genera of the oral Published: 31 March 2020 microbiota, such as Granulicatella, Parvimonas, and Streptococcus, suggesting the Citation: existence of a horizontally transferrable gene reservoir in the oral environment, likely García López E and Martín-Galiano AJ (2020) The facilitated by close proximity in biofilms and ultimately linked to endocarditis. The Versatility of Opportunistic Infections identification of the Gemella virulence pool should be implemented in whole genome- Caused by Gemella Isolates Is Supported by the Carriage based protocols to rationally predict the pathogenic potential in ongoing clinical of Virulence Factors From Multiple infections caused by these poorly known bacterial pathogens. Origins. Front. Microbiol. 11:524. doi: 10.3389/fmicb.2020.00524 Keywords: emergent pathogen, Granulicatella, horizontal gene transfer, Parvimonas, virulence factor Frontiers in Microbiology| www.frontiersin.org 1 March 2020| Volume 11| Article 524 fmicb-11-00524 March 27, 2020 Time: 17:39 # 2 García López and Martín-Galiano Genomic Basis for Gemella Infections INTRODUCTION could be used to complement WGS as a rapid initial analysis tool until WGS data are generated (Quainoo et al., 2017). Opportunistic pathogens are organisms that can become A very recent study has highlighted the appropriateness of pathogenic only after certain perturbations to the host, such WGS to investigate the presence of microorganisms (including as disease or injury prior infection, alteration of the immune Gemellae) in biopsies from patients with endophthalmitis system, or aging (Brown et al., 2012). Such species may (Deshmukh et al., 2019). have remained overlooked in the clinical setting due to their Currently, G. haemolysans is the type species of the genus intrinsic difficulty in being identified by ordinary microbiological which currently contains eleven different species (last date and/or molecular methods. Nevertheless, the advent of new accessed, 10 January 2020); these include nine species with techniques for the identification of bacterial species, such as standing in nomenclature (Parte, 2018) and two more recently matrix-assisted laser desorption ionization–time of flight mass described species (“Gemella massiliensis”) (Fonkou et al., 2018) spectrometry (MALDI-TOF MS), has been instrumental in and “Gemella muriseptica”(Eaton et al., 2019). Gemella isolates detecting infections caused by unusual pathogens (Seng et al., have been found as commensals in metagenomic approaches 2013). The implementation of other techniques such as whole- of the oral cavity, the upper respiratory tract, the intestine, genomic sequencing of bacterial clinical isolates, is greatly the breastmilk of healthy mothers and the female genital encouraged to increase identification resolution, particularly with tracts of humans (van de Wijgert et al., 2014; Boix-Amorós rare bacteria (Quainoo et al., 2017). et al., 2016; Takayasu et al., 2017; Esposito and Principi, 2018; Gemella sp. represents one of the bacterial groups that Villmones et al., 2018). exemplify the irruption of relatively frequent, opportunistic Gemellae are related to the Mitis and Salivarius groups of pathogens in the clinical laboratory. Gemellae are facultatively streptococci (Facklam and Elliott, 1995; Ruoff, 2002) that are anaerobic, cytochrome oxidase- and catalase-negative Gram- also members of the oral microbiota. These streptococci, such positive cocci with a DNA GCC content (mol%) as low as as Streptococcus gordonii, Streptococcus mitis, and Streptococcus 30–34 (Collins and Falsen, 2015). Bacterial species are commonly sanguinis, are well-known opportunistic pathogens able to defined by applying a set of predetermined criteria, most cause invasive diseases like sepsis and endocarditis (Abranches frequently including phenotypic data and 16S rRNA gene et al., 2018). Notably, Gemella carriage has also been associated sequence similarity. When required, DNA–DNA hybridization with allergies and asthma in children (Dzidic et al., 2018). experiments as well as genome-based criteria such as average Evidence of horizontal gene transfer (HGT) to Gemella of some nucleotide identity (ANI) are also employed. The identification genes associated with virulence in related streptococci is being of Gemella isolates represents a challenge to clinical laboratories. accumulated. These include genes encoding mainly paralogous Manual or commercial phenotypic methods may result in zinc metalloproteases (namely iga, zmpB, and zmpC) from misidentification of Gemella spp. as viridans group streptococci Streptococcus sp. (Takenouchi-Ohkubo et al., 2006; Bek-Thomsen or other related organisms and vice versa (Christensen and et al., 2012). Ruoff, 2015). Also 16S rRNA gene sequencing is frequently Despite this information, a detailed study of the employed to identify these microorganisms (Woo et al., 2003 virulence potential of Gemella spp. at a genomic scale is, and references therein). To date, 98.65% 16S rRNA gene to the best of our knowledge, lacking. Gemella genomic sequence similarity is the threshold for differentiating two sequences have been produced since the first sequence species (Kim et al., 2014). It is noteworthy that, for example, reported in 2008. With the aim of closing the current gap the type strains of Gemella parahaemolysans (NTUH_1465T) between genome availability and acquisition of biological and Gemella taiwanensis (NTUH_5572T) displayed 99.77 and value for this pathogen, a global genome analysis and 100% 16S rRNA gene sequence similarity with Gemella identification of potential virulence factors have been haemolysans ATCC 10379T (Hung et al., 2014). In such cases, approached in the present study. Results may help to phylogenetic analysis of concatenated sequences of two or understand the pathogenicity of the Gemella genus in more housekeeping genes must be performed for a detailed opportunistic infections. identification (Hung et al., 2010). Nevertheless, if a pathogen cannot be identified by conventional methods, MALDI-TOF MS should be considered (Welker et al., 2019), although it MATERIALS AND METHODS should be noted that some rare isolates may not be included in the database at the time of analysis (Fonkou et al., 2018). Literature Search Inconsistencies with MALDI-TOF MS results based on potential Reports were detected by searching the term “Gemella” in biases in phenotypic typing data from various protein expression PubMed (last date accessed, December 31, 2018), followed by levels must also be considered. Even though MALDI-TOF manual revision to verify unequivocal case reports involving MS was able to distinguish outbreak strains with shorter Gemella spp. without considering co-infections. turnaround times, whole-genome sequencing (WGS) analysis provided far-higher discriminatory power (recently reviewed Genome and Proteome Management by Hayashi Sant’Anna et al., 2019), which ultimately allowed All the original genomic and proteomic information was an improved understanding of transmission events. It has downloaded from the ASSEMBLY
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