Living in an Extremely Polluted Environment: Clues from the Genome of Melanin-Producing Aeromonas salmonicida subsp. pectinolytica 34melT

Abstract

Aeromonas salmonicida subsp. pectinolytica 34melT can be considered an extremophile due to the characteristics of the heavily polluted river from which it was isolated. While four subspecies of A. salmonicida are known fish pathogens, 34melT belongs to the only subspecies isolated solely from the environment. Genome analysis revealed high metabolic versatility, the capability to cope with diverse stress agents, and the lack of several virulence factors found in pathogenic Aeromonas. The most relevant phenotypic characteristics of 34melT are pectin degradation, a distinctive trait of the pectinolytica subspecies, and melanin production. Genes coding for three pectate lyases were detected in a cluster unique for this microorganism, that contains all genes needed for pectin degradation. Melanin synthesis in 34melT is hypothesized to occur through the homogentisate pathway, as no tyrosinases or laccases were detected, and the homogentisate 1,2-dioxygenase gene is inactivated by a transposon insertion, leading to the accumulation of the melanin precursor homogentisate. Comparative genome analysis of other melanogenic Aeromonas revealed that this gene was inactivated by transposon insertions or point mutations, indicating that melanin biosynthesis in Aeromonas occurs through the homogentisate pathway. Horizontal gene transfer could have contributed to the adaptation of 34melT to a highly polluted environment, as thirteen genomic islands were identified in its genome, some of them containing genes coding for fitness related traits. Heavy metal resistance genes, along with others associated to oxidative and nitrosative stress were also found. These characteristics, together with melanin production and the ability to use different substrates, could explain the capability of this microorganism to live in an extremely polluted environment.