Affiliation:
1. Department of Biomedicine, Faculty of Health, Aarhus University, Aarhus, Denmark
2. Department of Microbiology and Immunology, Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA
Abstract
ABSTRACT
The bacterium
Streptococcus pneumoniae
is one of the leading causes of fatal infections affecting humans. Intriguingly, phylogenetic analysis shows that the species constitutes one evolutionary lineage in a cluster of the otherwise commensal
Streptococcus mitis
strains, with which humans live in harmony. In a comparative analysis of 35 genomes, including phylogenetic analyses of all predicted genes, we have shown that the pathogenic pneumococcus has evolved into a master of genomic flexibility while lineages that evolved into the nonpathogenic
S. mitis
secured harmonious coexistence with their host by stabilizing an approximately 15%-reduced genome devoid of many virulence genes. Our data further provide evidence that interspecies gene transfer between
S. pneumoniae
and
S. mitis
occurs in a unidirectional manner, i.e., from
S. mitis
to
S. pneumoniae
. Import of genes from
S. mitis
and other mitis, anginosus, and salivarius group streptococci ensured allelic replacements and antigenic diversification and has been driving the evolution of the remarkable structural diversity of capsular polysaccharides of
S. pneumoniae
. Our study explains how the unique structural diversity of the pneumococcal capsule emerged and conceivably will continue to increase and reveals a striking example of the fragile border between the commensal and pathogenic lifestyles. While genomic plasticity enabling quick adaptation to environmental stress is a necessity for the pathogenic streptococci, the commensal lifestyle benefits from stability.
IMPORTANCE
One of the leading causes of fatal infections affecting humans,
Streptococcus pneumoniae
, and the commensal
Streptococcus mitis
are closely related obligate symbionts associated with hominids. Faced with a shortage of accessible hosts, the two opposing lifestyles evolved in parallel. We have shown that the nonpathogenic
S. mitis
secured harmonious coexistence with its host by stabilizing a reduced genome devoid of many virulence genes. Meanwhile, the pathogenic pneumococcus evolved into a master of genomic flexibility and imports genes from
S. mitis
and other related streptococci. This process ensured antigenic diversification and has been driving the evolution of the remarkable structural diversity of capsular polysaccharides of
S. pneumoniae
, which conceivably will continue to increase and present a challenge to disease prevention.
Publisher
American Society for Microbiology