Open Access Research article

Comparative genomics of the dairy isolate Streptococcus macedonicus ACA-DC 198 against related members of the Streptococcus bovis/Streptococcus equinus complex

Konstantinos Papadimitriou1*, Rania Anastasiou1, Eleni Mavrogonatou2, Jochen Blom3, Nikos C Papandreou4, Stavros J Hamodrakas4, Stéphanie Ferreira5, Pierre Renault67, Philip Supply1011589, Bruno Pot101189 and Effie Tsakalidou1

Author Affiliations

1 Laboratory of Dairy Research, Department of Food Science and Human Nutrition, Agricultural University of Athens, Iera Odos 75, Athens 118 55, Greece

2 Laboratory of Cell Proliferation and Ageing, Institute of Biosciences and Applications, National Centre for Scientific Research "Demokritos", Athens 153 10, Greece

3 Computational Genomics, Center for Biotechnology, Bielefeld University, Bielefeld, Germany

4 Department of Cell Biology and Biophysics, Faculty of Biology, University of Athens, Panepistimiopolis, Athens 157 01, Greece

5 Genoscreen, Genomic Platform and R&D, Campus de l’Institut Pasteur, 1 rue du Professeur Calmette, Lille 59000, France

6 INRA, UMR1319 Micalis, Jouy-en-Josas F-78352, France

7 AgroParisTech, UMR Micalis, Jouy-en-Josas F-78352, France

8 Institut Pasteur de Lille, Center for Infection and Immunity of Lille (CIIL), Lille F-59019, France

9 Inserm U1019, F-59019 Lille, France

10 CNRS UMR8204, Lille F-59021, France

11 Univ Lille de Nord France, Lille F-59000, France

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BMC Genomics 2014, 15:272  doi:10.1186/1471-2164-15-272

Published: 8 April 2014

Abstract

Background

Within the genus Streptococcus, only Streptococcus thermophilus is used as a starter culture in food fermentations. Streptococcus macedonicus though, which belongs to the Streptococcus bovis/Streptococcus equinus complex (SBSEC), is also frequently isolated from fermented foods mainly of dairy origin. Members of the SBSEC have been implicated in human endocarditis and colon cancer. Here we compare the genome sequence of the dairy isolate S. macedonicus ACA-DC 198 to the other SBSEC genomes in order to assess in silico its potential adaptation to milk and its pathogenicity status.

Results

Despite the fact that the SBSEC species were found tightly related based on whole genome phylogeny of streptococci, two distinct patterns of evolution were identified among them. Streptococcus macedonicus, Streptococcus infantarius CJ18 and Streptococcus pasteurianus ATCC 43144 seem to have undergone reductive evolution resulting in significantly diminished genome sizes and increased percentages of potential pseudogenes when compared to Streptococcus gallolyticus subsp. gallolyticus. In addition, the three species seem to have lost genes for catabolizing complex plant carbohydrates and for detoxifying toxic substances previously linked to the ability of S. gallolyticus to survive in the rumen. Analysis of the S. macedonicus genome revealed features that could support adaptation to milk, including an extra gene cluster for lactose and galactose metabolism, a proteolytic system for casein hydrolysis, auxotrophy for several vitamins, an increased ability to resist bacteriophages and horizontal gene transfer events with the dairy Lactococcus lactis and S. thermophilus as potential donors. In addition, S. macedonicus lacks several pathogenicity-related genes found in S. gallolyticus. For example, S. macedonicus has retained only one (i.e. the pil3) of the three pilus gene clusters which may mediate the binding of S. gallolyticus to the extracellular matrix. Unexpectedly, similar findings were obtained not only for the dairy S. infantarius CJ18, but also for the blood isolate S. pasteurianus ATCC 43144.

Conclusions

Our whole genome analyses suggest traits of adaptation of S. macedonicus to the nutrient-rich dairy environment. During this process the bacterium gained genes presumably important for this new ecological niche. Finally, S. macedonicus carries a reduced number of putative SBSEC virulence factors, which suggests a diminished pathogenic potential.

Keywords:
Streptococcus; Genome; Adaptation; Gene decay; Pseudogene; Horizontal gene transfer; Pathogenicity; Virulence factor; Milk; Niche