Comparative genome analysis of Streptococcus infantarius subsp. infantariusCJ18, an African fermented camel milk isolate with adaptations to dairy environment

Christoph Jans,Christophe Lacroix,Mira Hochstrasser,Rainer Follador,Leo Meile,Marc J A Stevens

doi:10.1186/1471-2164-14-200

Abstract

BackgroundStreptococcus infantarius subsp. infantarius (Sii) belongs to the Streptococcus bovis/Streptococcus equinus complex associated with several human and animal infections. Sii is a predominant bacterium in spontaneously fermented milk products in Africa. The genome sequence of Sii strain CJ18 was compared with that of other Streptococcus species to identify dairy adaptations including genome decay such as in Streptococcus thermophilus, traits for its competitiveness in spontaneous milk fermentation and to assess potential health risks for consumers.ResultsThe genome of Sii CJ18 harbors several unique regions in comparison to Sii ATCC BAA-102T, among others an enlarged exo- and capsular polysaccharide operon; Streptococcus thermophilus-associated genes; a region containing metabolic and hypothetical genes mostly unique to CJ18 and the dairy isolate Streptococcus gallolyticus subsp. macedonicus; and a second oligopeptide transport operon. Dairy adaptations in CJ18 are reflected by a high percentage of pseudogenes (4.9%) representing genome decay which includes the inactivation of the lactose phosphotransferase system (lacIIABC) by multiple transposases integration. The presence of lacS and lacZ genes is the major dairy adaptation affecting lactose metabolism pathways also due to the disruption of lacIIABC.We constructed mutant strains of lacS, lacZ and lacIIABC and analyzed the resulting strains of CJ18 to confirm the redirection of lactose metabolism via LacS and LacZ.Natural competence genes are conserved in both Sii strains, but CJ18 contains a lower number of CRISPR spacers which indicates a reduced defense capability against alien DNA. No classical streptococcal virulence factors were detected in both Sii strains apart from those involved in adhesion which should be considered niche factors. Sii-specific virulence factors are not described. Several Sii-specific regions encoding uncharacterized proteins provide new leads for virulence analyses and investigation of the unclear association of dairy and clinical Sii with human diseases.ConclusionsThe genome of the African dairy isolate Sii CJ18 clearly differs from the human isolate ATCC BAA-102T. CJ18 possesses a high natural competence predisposition likely explaining the enlarged genome. Metabolic adaptations to the dairy environment are evident and especially lactose uptake corresponds to S. thermophilus. Genome decay is not as advanced as in S. thermophilus (10-19%) possibly due to a shorter history in dairy fermentations.

Highlights

Streptococcus infantarius subsp. infantarius (Sii) belongs to the Streptococcus bovis/Streptococcus equinus complex associated with several human and animal infections
Sii belongs to the Lancefield group D Streptococcus bovis/ Streptococcus equinus complex (SBSEC) which comprises the species S. bovis, S. equinus, Streptococcus lutetiensis, Streptococcus gallolyticus subsp. gallolyticus, Streptococcus gallolyticus subsp. macedonicus, Streptococcus gallolyticus subsp. pasteurianus and Streptococcus alactolyticus [3,4,9]
The African dairy strain Sii CJ18 revealed many genetic adaptations to the dairy environment through acquired carbohydrate utilization pathways resulting in a lactose metabolism paralleling that of S. thermophilus

Summary

Introduction

Streptococcus infantarius subsp. infantarius (Sii) belongs to the Streptococcus bovis/Streptococcus equinus complex associated with several human and animal infections. Sii has been isolated from dairy products, feces (including the type strain ATCC BAA-102T and isogenetic strain CCUG 43820T), human blood (n = 3) and human endocarditis (n = 3) [2,3,4,5] It was identified as the predominant species in several spontaneously fermented African dairy products such as suusac, gariss and fènè [2,5,6,7] and in the Mexican fermented maize beverage pozol [8]. Potential virulence factors such as adhesion proteins have been shown e.g. the surface protein histone-like protein A (HlpA), the “adhesion to collagen of the S. bovis group” (Acb) and “S. bovis group surface protein” (Sbs) [14,20] Many of these factors seem to be necessary for survival of SBSEC in the gastrointestinal tract and should be considered as niche factors [21]

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