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Chapter 8 : Ecology and Evolution of Chromosomal Gene Transfer between Environmental Microorganisms and Pathogens

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Abstract:

The evolution of living beings is a complex process, with a large degree of serendipity, in which the offspring displace the ancestors. Indeed, what we find in the current multicellular world, and more specifically in the animal world, are the last members of an evolutionary process; all other members in the same branch of the phylogenetic tree have disappeared. In this regard, most multicellular organisms can be considered as newcomers on Earth, which have appeared quite recently in evolutionary terms. Although there are still some progenitors that stand after the evolution of their siblings, the most common scenario for multicellular organisms is that ancestors disappear once the evolved progeny displace them (see the evolution of ). This type of recent evolution followed by extinction is not so frequent in the case of bacterial species, although it may have happened on some occasions (see the example of described below). Indeed, the origin of different pathogens has been tracked to more than 100 million years ago, long before the human being (or an ancestor) was present on Earth ( ). Despite this extremely long evolutionary time, which should have allowed for large diversification with the loss of ancestors, bacterial core genomes are remarkably stable. It could be expected that the allelic variants of bacterial genes should cover nearly the entire potential spectrum of synonymous mutations and even those nonsynonymous mutations without substantial associated fitness costs. However, today we can use multilocus sequence typing for distinguishing among different clones in bacterial populations, under the assumption that, at least for several of the core genome genes, fixation of mutations is not a frequent event ( ). It then seems that, unless there is a major change in habitat, mutation-driven evolution is not the most important process in the speciation of bacteria in general, and in particular in the case of bacterial pathogens. A major force in such evolution, however, would be the acquisition of genetic elements ( ), what has been dubbed evolution in quantum leaps ( ). These acquired genes constitute the accessory genome of an organism and the pangenome of a given species ( ).

Citation: Martínez J. 2019. Ecology and Evolution of Chromosomal Gene Transfer between Environmental Microorganisms and Pathogens, p 141-160. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0006-2016
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Figure 1

Evolutionary trajectories of bacterial pathogens. (A) The process of speciation of a pathogen (larger circles) such as . This process usually begins with the acquisition, by HGT, of a set of genes (red circle) that allow the shift of the pathogen’s habitat from the environment to an infected host ( ). If the rate of transmission is high enough, the newborn pathogen will disseminate among different individuals ( ) and evolve by different mechanisms that include mutation and eventually genome reduction ( ). These evolutionary processes might cause the deadaptation of the pathogen to its original habitat, in which case the chances of the microorganism recolonizing natural ecosystems will be low ( ). Once the organism is a pathogen, it can change host specificity by acquiring novel genes ( ) and eventually by losing of determinants unneeded in the novel host ( ). In all cases, the integration of the acquired elements into the preformed bacterial metabolic and regulatory networks will be tuned by mutation. (B) The process of short-sighted evolution of opportunistic pathogens with an environmental origin, like . These microorganisms infect patients, presenting a basal disease, using virulence determinants already encoded in their genomes ( ). During chronic infection, the infective strain evolves mainly by mutation and genome rearrangements ( ). However, since it only infects people with a basal disease, transmission rates are usually low, which precludes clonal expansion and further diversification. Since adaptation to the new host is of no value for colonizing the environmental habitat ( ), this is a dead-end evolutionary process. (C) The evolution of pathogens such as that present virulence determinants with a dual role in the environment and for infections, in which case the colonization of one of these two habitats does not severely compromise the colonization of the other ( ). Reproduced with permission from reference .

Citation: Martínez J. 2019. Ecology and Evolution of Chromosomal Gene Transfer between Environmental Microorganisms and Pathogens, p 141-160. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0006-2016
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Image of Figure 2
Figure 2

Evolution of . The process of speciation from an environmental, nonpathogenic ancestor is a good example of the evolutionary steps that are involved in the emergence of bacterial pathogens. This process began with the acquisition of the plasmid pCD1 by environmental . This plasmid harbors genes encoding virulence determinants such as type III secretion systems and effector Yop proteins. From this ancestor of virulent species, two branches have evolved. One diverged through the acquisition of the stable toxin (Yst) and led to the speciation of . This species has further evolved through acquisition and loss of genes (not shown in this figure). The other branch diverged through the acquisition of the high pathogenicity island (HPI*), which encodes an iron-uptake system and is present as well in different , and by the incorporation of insecticidal genes. is a successful clone that emerged recently from through the acquisition of the plasmids pCP1, which encodes the plasminogen activator gene, and pMT1, which allows colonization of the gut of fleas. The loss of insect toxins is an important event for the persistence of in its insect vectors. The acquisition of insertion sequences is the basis of the genome rearrangements and gene loss of . Finally, the entire process of adaptation to a new host is modulated by the mutation-driven optimization of the regulatory and metabolic networks of the pathogen. This evolutionary process is described in more detail in references , and . Reproduced with permission from reference .

Citation: Martínez J. 2019. Ecology and Evolution of Chromosomal Gene Transfer between Environmental Microorganisms and Pathogens, p 141-160. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0006-2016
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Figure 3

Exaptation and gene decontextualization in the evolution of antibiotic resistance. Antibiotic resistance genes () have evolved for millions of years located in the chromosomes of their original hosts (a). During this evolution, the expression of these determinants (R) from their promoters (P) has been finely tuned to respond to several signals that might include the response to environmental and metabolic changes (blue arrows). Besides, the determinants encoded by these genes are integrated in physiological networks, where they can play a role as metabolic enzymes. S1 to S3 represent metabolites of the same pathway, and A1 and B1 metabolites of other interconnected pathways. When these genes are integrated in gene capture (for instance, an integron) and transfer units (for instance, a plasmid), they can be transferred to a new host and submitted to strong antibiotic selective pressure (b), and they can be constitutively expressed from a strong promoter (P) present in the capture unit and therefore lack the regulatory and physiological network encountered in the original host (gene decontextualization). Under these circumstances, the only function these determinants can play is antibiotic resistance, in such a way that this functional shift is not the consequence of adaptive changes in the determinants but rather of changes in their environment (exaptation). Reproduced with permission from reference .

Citation: Martínez J. 2019. Ecology and Evolution of Chromosomal Gene Transfer between Environmental Microorganisms and Pathogens, p 141-160. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0006-2016
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