The gene cassette metagenome is a basic resource for bacterial genome evolution

Abstract

Lateral gene transfer has been proposed as a fundamental process underlying bacterial diversity. Transposons, plasmids and phage are widespread and have been shown to significantly contribute to lateral gene transfer. However, the processes by which disparate genes are assembled and integrated into the host regulatory network to yield new phenotypes are poorly known. Recent discoveries about the integron/gene cassette system indicate it has the potential to play a role in this process. Gene cassettes are small mobile elements typically consisting of a promoterless orf and a recombination site. Integrons are capable of acquisition and re-arrangement of gene cassettes and of the expression of their associated genes. The potential of the integron/gene cassette system is thus largely determined by the diversity contained within the cassette pool and the rate at which integrons sample this pool. We show here using a polymerase chain reaction (PCR) approach by which the environmental gene cassette (EGC) metagenome can be directly sampled that this metagenome contains both protein-coding and non-protein coding genes. Environmental gene cassette-associated recombination sites showed greater diversity than previously seen in integron arrays. Class 1 integrons were shown to be capable of accessing this gene pool through tests of recombinational activity with a representative range of EGCs. We propose that gene cassettes represent a vast, prepackaged genetic resource that could be thought of as a metagenomic template for bacterial evolution.

Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter

“…AttI inserts from three genera on two farms were gene fragments, as also recently noted in a large survey of soil communities (ref. 43; Table 4). We do not have qPCR data for Farms 3 and 4, but aadA occurred in all isolates from these farms, indicating that Class 1 integron carriage by abundant aerobic Gram-positive bacteria in poultry litter is not unique to Farms 1 and 2.…”

Use of chromosomal integron arrays as a phylogenetic typing system for Vibrio cholerae pandemic strains

“…Thus, the ability of the method described here to identify the presence or absence of specific gene cassettes has applications in evaluating the MGC pool available to V. cholerae. MGCs are a vast source of genetic diversity (Holmes et al, 2003), and a source of new phenotypes, including pathogenicity. For example, a 1099 bp MGC (MGC133 in N16961) in V. cholerae encodes a mannose-resistant haemagglutinin that is an important colonization factor (Barker & Clark, 1994;Franzon et al, 1993).…”

Bacteria are small but not stupid: cognition, natural genetic engineering and socio-bacteriology

“…Integrons are not limited to antibiotic resistance determinants. A large "super-integron" encoding pathogenicity determinants was discovered in the genome of Vibrio cholerae (Mazel et al, 1998), and diverse bacteria have integrons or sequences for the integrase protein that mediates cassette insertion and excision (Holmes et al, 2003). The functional significance of the cassettes in these novel integrons is not known, but less than 5% show similarity to antibiotic resistance functions (Holmes et al, 2003).…”