Metagenomic assessment of the interplay between the environment and the genetic diversification of Acinetobacter

Abstract

SummaryMost bacteria have poorly characterized environmental reservoirs and unknown closely related species. This hampers the study of bacterial evolutionary ecology because both the environment and the genetic background of ancestral lineages are unknown. We combined metagenomics, comparative genomics and phylogenomics to overcome this limitation, to identify novel taxa and to propose environments where they can be isolated. We applied this method to characterize the ecological distribution of known and novel lineages of Acinetobacter spp. We observed two major environmental transitions at deep phylogenetic levels, splitting the genus into three ecologically differentiated clades. One of these has rapidly shifted towards host‐association by acquiring genes involved in bacteria‐eukaryote interactions. We show that environmental perturbations affect species distribution in predictable ways: bovines have very diverse communities of Acinetobacter, unless they were administered antibiotics, in which case they show highly uniform communities of Acinetobacter spp. that resemble those of humans. Our results uncover the diversity of bacterial lineages, overpassing the limitations of classical cultivation methods and highlight the role of the environment in shaping their evolution.

Microevolution in the major outer membrane protein OmpA ofAcinetobacter baumannii

“…The main difference between them resides in the presence/absence of a hydrophobic tract of 6 amino acids composed mostly by alanine residues close to the C-terminal end (Figure 2B). We noted that the DNA sequence coding this tract, 5’-GCGGCAGCTCCTGCAGCA-3’, shows a higher GC content (72 %) when compared to the rest of the A. baumannii ompA gene (42 %) or even to the average GC content of Acinetobacter genomes (1–6). This suggests that the long QEAAAPAAAQ C-terminal region may have derived from a non-homologous (illegitimate) recombination event involving the insertion of a fragment originating in a high-GC DNA source outside the Acinetobacter genus (43–46).…”

“…This suggests that the long QEAAAPAAAQ C-terminal region may have derived from a non-homologous (illegitimate) recombination event involving the insertion of a fragment originating in a high-GC DNA source outside the Acinetobacter genus (43–46). Moreover, this event is likely to have been selected recently in A. baumannii or in a related ACB complex species, as judged by the presence of OmpAs bearing QEAAAPAAAQ as C-terminal ends only among A. baumannii and other ACB species (Table S2) but not the other ecologically-differentiated clades (Table S4) into which the Acinetobacter genus was recently divided (1).…”

“…The genus Acinetobacter (family Moraxellaceae , class Gammaproteobacteria ) is composed of Gram-negative bacterial organisms of ubiquitous environmental distribution (1). It includes a number of phylogenetically closely-related species generally associated with the human environment grouped into the so-called Acinetobacter calcoaceticus/Acinetobacter baumannii complex (ACB).…”

“…It includes a number of phylogenetically closely-related species generally associated with the human environment grouped into the so-called Acinetobacter calcoaceticus/Acinetobacter baumannii complex (ACB). Of these, A. baumannii represents the most problematic nosocomial species generally affecting critically-ill patients (1–6). Molecular typing studies have indicated that infective A. baumannii strains belong to a limited number of globally-distributed clonal groups/complexes (CCs) of recent emergence (2–9).…”

“…Molecular typing studies have indicated that infective A. baumannii strains belong to a limited number of globally-distributed clonal groups/complexes (CCs) of recent emergence (2–9). The reasons for the success of CC strains as human pathogens are still poorly understood, but are thought to include the general resilience of the species, an increased ability to colonize the human environment, and their propensity to acquire exogenous genetic material (1–9). Thus, CC strains not only show multi-drug resistance (MDR) phenotypes from the acquisition of different mobile genetic elements enriched in resistance genes, but can also rapidly modify virulence-related surface structures recognized by host defenses as the result of recombination events involving discrete genomic loci (2–6, 9–12).…”