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. 2017 Apr 4;17(1):94.
doi: 10.1186/s12862-017-0942-y.

Reconstruction of the Evolution of Microbial Defense Systems

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Free PMC article

Reconstruction of the Evolution of Microbial Defense Systems

Pere Puigbò et al. BMC Evol Biol. .
Free PMC article

Abstract

Background: Evolution of bacterial and archaeal genomes is a highly dynamic process that involves intensive loss of genes as well as gene gain via horizontal transfer, with a lesser contribution from gene duplication. The rates of these processes can be estimated by comparing genomes that are linked by an evolutionary tree. These estimated rates of genome dynamics events substantially differ for different functional classes of genes. The genes involved in defense against viruses and other invading DNA are among those that are gained and lost at the highest rates.

Results: We employed a stochastic birth-and-death model to obtain maximum likelihood estimates of the rates of gain and loss of defense genes in 35 groups of closely related bacterial genomes and one group of archaeal genomes. We find that on average, the defense genes experience 1.4 fold higher flux than the rest of microbial genes. This excessive flux of defense genes over the genomic mean is consistent across diverse microbial groups. The few exceptions include intracellular parasites with small, degraded genomes that possess few defense systems which are more stable than in other microbes. Generally, defense genes follow the previously established pattern of genome dynamics, with gene family loss being about 3 times more common than gain and an order of magnitude more common than expansion or contraction of gene families. Case by case analysis of the evolutionary dynamics of defense genes indicates frequent multiple events in the same locus and widespread involvement of mobile elements in the gain and loss of defense genes.

Conclusions: Evolution of microbial defense systems is highly dynamic but, notwithstanding the host-parasite arms race, generally follows the same trends that have been established for the rest of the genes. Apart from the paucity and the low flux of defense genes in parasitic bacteria with deteriorating genomes, there is no clear connection between the evolutionary regime of defense systems and microbial life style.

Figures

Fig. 1
Fig. 1
Correlation of COGs and defense systems. a All COGs vs. number of defense systems. b All COGs vs. percentage of defense systems. Each figure contains 36 dots each of which represents an ATGC. The ATGCs discussed in the text are indicated in panel b
Fig. 2
Fig. 2
Distribution of defense systems across the species tree. a The tree was reconstructed using data from MicrobesOnline [56]. Length of bars is proportional to the number of defense systems. b Distribution of the relative abundance of defense systems in the ATGC
Fig. 3
Fig. 3
Number of genes assigned to defense systems (N_DS) and genome dynamics by type of defense system. a Number of defense genes (COGs) distributed by type of defense systems. b Number of genome dynamic events (GDE), including gain, loss, expansion and reduction, by type of defense systems
Fig. 4
Fig. 4
Correlation of genome dynamics events normalized by number of COGs of all genes vs. defense systems. a Gain. b Loss. c Expansion. d Reduction
Fig. 5
Fig. 5
Density plots of rates of genome dynamics in defense systems normalized by the rates in all genes. a Distribution in all ATGCs. b Distribution in Actinobacteria, Firmicutes and Proteobacteria. c Distribution in free living (FL) and facultative host associated (FHA) bacteria
Fig. 6
Fig. 6
Principal components analysis of the relative rates of gain, loss, expansion and reduction in defense systems normalized by the rates in all genes. a PCA plot. Each dot corresponds to an ATGC. b Loadings plot. c Bar plot of the PCA’s main principal components by ATGC
Fig. 7
Fig. 7
Examples of defense gene gain. The trees for the ATGC genomes, reconstructed from concatenated alignments of nucleotide sequences of common orthologs [29] are shown in the left part of each panel. Defense system loci are schematically depicted in the right part of each panel. Homologous genes are highlighted in matching colors. Genes that are rare or unique in these regions are shown as blank shapes. Genes are labeled by the gene names or by NCBI CDD profile names. Gained genes are shown by red outline. Conserved flanking genes are shown by blue outline. a Acquisition of RM-related genes in Corynebacterium diphtheriae BH8. b Recombination in situ in the CRISPR-cas locus of Clostridium botulinum strains. The cas genes and CRISPR-Cas system subtypes are labeled according to the current CRISPR-Cas system classification and nomenclature [34]. The cas6 gene not affected by recombination are is highlighted by yellow outline. The phylogenetic tree for the cas6 nucleotide sequences is schematically shown opposite the genome tree. c Acquisition of Abi genes in the Propionibacterium acnes strains SK137 and HL096PA1

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