From Environment to Man: Genome Evolution and Adaptation of Human Opportunistic Bacterial Pathogens

Abstract

Environment is recognized as a huge reservoir for bacterial species and a source of human pathogens. Some environmental bacteria have an extraordinary range of activities that include promotion of plant growth or disease, breakdown of pollutants, production of original biomolecules, but also multidrug resistance and human pathogenicity. The versatility of bacterial life-style involves adaptation to various niches. Adaptation to both open environment and human specific niches is a major challenge that involves intermediate organisms allowing pre-adaptation to humans. The aim of this review is to analyze genomic features of environmental bacteria in order to explain their adaptation to human beings. The genera Pseudomonas , Aeromonas and Ochrobactrum provide valuable examples of opportunistic behavior associated to particular genomic structure and evolution. Particularly, we performed original genomic comparisons among aeromonads and between the strictly intracellular pathogens Brucella spp. and the mild opportunistic pathogens Ochrobactrum spp. We conclude that the adaptation to human could coincide with a speciation in action revealed by modifications in both genomic and population structures. This adaptation-driven speciation could be a major mechanism for the emergence of true pathogens besides the acquisition of specialized virulence factors.

Recent independent emergence of multiple multidrug-resistantSerratia marcescensclones within the United Kingdom and Ireland

“…S. marcescens was previously believed to be a nonpathogenic environmental species but has been recognized as an increasingly important opportunistic pathogen over the past few decades (Mahlen 2011). The large accessory genome and genomic flexibility is likely to be important for its ability to act as an opportunistic pathogen (Aujoulat et al 2012).…”

Aeromonas spp.: ubiquitous or specialized bugs?

“…produce an impressive array of virulence factors whose role in human pathogenicity is still unclear, and there is no standard terminology regarding these factors (Chopra et al ., ). It also has been reported that the actual role of Aeromonas virulence factors may be unrelated to typical virulence mechanisms, particularly towards humans, but instead are involved in sensing and responding to signals originating from the host environment (Aujoulat et al ., ). Grim and colleagues () have compared the genomic sequences of four A. hydrophila strains, identifying some virulence factors that could enhance Aeromonas pathogenicity, but a large‐scale evaluation is still necessary.…”

“…Aeromonas is mainly isolated from the gastrointestinal tract, but an increasing number of cases of Aeromonas ‐associated extra‐intestinal diseases has been documented worldwide (Thomsen and Kristianse, ; Sarma, ; Cigni et al ., ; Mencacci et al ., ; Lamy et al ., ). Water is considered the most frequent source of human infection (Aujoulat et al ., ), but aeromonads can also be contracted by other routes, such as the ingestion of contaminated foods. The inability to assess, with certainty, the pathogenicity of Aeromonas towards humans is attributable to multiple factors: the lack of an animal model that can faithfully reproduce the Aeromonas ‐associated syndromes, although many attempts have been made (Kelleher and Kirov, ); the inability to fulfil Koch's postulates (Evans, ); and the failure to identify a single clonally related outbreak of disease caused by these bacteria (Janda and Abbott, ).…”

Pyomelanin‐producing Pseudomonas aeruginosa selected during chronic infections have a large chromosomal deletion which confers resistance to pyocins

“…Pseudomonas aeruginosa is an extremely common opportunistic pathogen. Its large genome (6.5 Mbp) accounts for its metabolic versatility and affinity for various environmental niches, but also for its infectious capability towards a large set of hosts (Aujoulat et al, 2012). P. aeruginosa is a leading cause of hospital-acquired infections.…”