A multi-omics perspective on the biology and evolution of the genus Macrococcus

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Mazhar, Shahneela
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University College Cork
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The Gram-positive genus Macrococcus currently comprises eleven species; Macrococcus bovicus, Macrococcus carouselicus, Macrococcus equipercicus, Macrococcus brunensis, Macrococcus hajekii, Macrococcus lamae, Macrococcus goetzii, Macrococcus bohemicus, Macrococcus epidermidis, Macrococcus canis, and Macrococcus caseolyticus that are commonly isolated from animal skin and their meat and milk products. The species of this genus are evolutionarily closely related to the species of Staphylococcus. In contrast to staphylococcal species, macrococci are generally thought to be avirulent. However, new evidence suggests the emergence of the species M. caseolyticus as a potential new pathogen. Additionally, genomic insights into the genomes of some members of this genus demonstrate the potential for these organisms to serve as reservoirs of methicillin resistance determinants. Considering that strains of the M. caseolyticus species have been associated with flavour development in dairy and fermented meat products, further investigation of this fascinating genus, and the species within it, is warranted. Therefore, this thesis aimed to explore genus-wide genomic diversity and distribution of antimicrobial resistance along with examining the role of M. caseolyticusin the flavour development of fermented dairy products, paying particular attention to the safety of this organism in the food system. During this thesis work, a rapid PCR-based method was developed to isolate and establish a strain collection of M. caseolyticus and M. canis from diverse sources. The 13 strains isolated in this study were investigated using phylogenetic analysis based on partial 16S rRNA and ctaC gene, revealed DPC7161T strain to form a separate branch from all the known members of the genus. A polyphasic approach based on the combination of genomic, phenotypic, and chemotaxonomic characteristics were used to identify the taxonomic position of DPC7161T. The results from this analysis suggested that strain DPC7161T represents a novel species of the genus Macrococcus with the name Macrococcus linguae sp. nov, proposed. Further comparative genomics analysis suggested that M. goetzii and M. canis species are composed of two distinct subspecies: M. canis subsp. canis subsp. nov., M. canis subsp. bovinus subsp. nov., M. goetzii subsp. goetzii subsp. nov, and M. goetzii subsp. corkensis subsp. nov. After a thorough taxonomic characterisation of strain collection, six strains belonging to the M. caseolyticus species were further investigated using a systems wide approach integrating the enzymatic, metabolic and genomic data to unravel their flavour forming potential. The enzymatic analysis has identified highly active cell wall bound proteases driving extensive casein hydrolysis associated with dairy-derived strains of M. caseolyticus. Finally, pan-genomic analysis revealed considerable genetic diversity within the genus Macrococcus. The presence of antimicrobial resistance genes on genomic islands associated with mobile genetic elements suggests horizontal gene transfer as a key driver in the spread of antimicrobial resistance genes across the members of this genus. Overall, this thesis presents the genomic and metabolic diversity within the genus Macrococcus and the potential application of M. caseolyticus in flavour diversification.
Macrococcus , Methicillin resistance , Evolution , Staphylococcus , Comparative genomics , Mobile genetic elements , Horizontal gene transfer
Mazhar, S. 2020. A multi-omics perspective on the biology and evolution of the genus Macrococcus. PhD Thesis, University College Cork.