Horizontal Gene Transfer as a Source of Conflict and Cooperation in Prokaryotes

Abstract

Horizontal gene transfer (HGT) is one of the most important processes in prokaryote evolution. The sharing of DNA can spread neutral or beneficial genes, as well as genetic parasites across populations and communities, creating a large proportion of the variability acted on by natural selection. Here, we highlight the role of HGT in enhancing the opportunities for conflict and cooperation within and between prokaryote genomes. We discuss how horizontally acquired genes can cooperate or conflict both with each other and with a recipient genome, resulting in signature patterns of gene co-occurrence, avoidance, and dependence. We then describe how interactions involving horizontally transferred genes may influence cooperation and conflict at higher levels (populations, communities, and symbioses). Finally, we consider the benefits and drawbacks of HGT for prokaryotes and its fundamental role in understanding conflict and cooperation from the gene-gene to the microbiome level.

Keywords: antimicrobial resistance; conflict; cooperation; horizontal gene transfer; natural selection.

Figure 1

Schematic description of the agents considered in this article, with examples of some of their interactions. Shapes indicate the type of agent, while color represents the type of interaction. Agents of the same color cooperate, and agents of different colors conflict with one another. (A) Acquisition of three genes allows the teal bacteria to colonize a niche dominated by the yellow bacteria (1). The yellow bacteria, however, produce an antibiotic capable of killing the teal cells (2). In this novel environment, teal bacteria have acquired a plasmid encoding an antibiotic-degrading enzyme (3), which allows them to expand their population. (B) The antibiotic producing gene can be acquired by transduction in new cells (4). Selfish phage can also insert in the chromosome (5). Transformation followed by homologous recombination can eliminate selfish elements from the chromosome (6) but can also lead to gain of selfish elements (7), in this case by illegitimate recombination. (C) In some backgrounds, these selfish elements can expand, increasing the chance of insertion in essential parts of the genome (8). These elements can also insert in conjugative plasmids, which can then be transmitted to other cells (8 and 9). Among the population of teal cells, cheats arise that do not produce the antibiotic degrading enzyme (10). (D) Reacquisition of the enzyme encoding plasmid by conjugation restores cooperation, although it also introduces the selfish element (11). The expansion of selfish elements results in the death of the yellow cell (12), as the teal population continues to expand.