Evolutionary Ecology of Prokaryotic Immune Mechanisms

Abstract

Bacteria have a range of distinct immune strategies that provide protection against bacteriophage (phage) infections. While much has been learned about the mechanism of action of these defense strategies, it is less clear why such diversity in defense strategies has evolved. In this review, we discuss the short- and long-term costs and benefits of the different resistance strategies and, hence, the ecological conditions that are likely to favor the different strategies alone and in combination. Finally, we discuss some of the broader consequences, beyond resistance to phage and other genetic elements, resulting from the operation of different immune strategies.

FIG 1

Bacterial immune mechanisms. Letters indicate protein components involved in the immune mechanism (M, methylase; R, restriction enzyme; C1/2, Cas1 and Cas2; C, Cas effector-nuclease complex; A, prokaryotic Argonaute enzyme).

FIG 2

Four-dimensional space defined by the four axes that capture different features of immune mechanisms is sufficient to explain the existing diversity of immune mechanisms in nature. The ecological factors indicated drive the evolution of the feature indicated on the corresponding axis. Details are provided in the text.

FIG 3

The force of infection is an important determinant of the relative fitness associated with CRISPRs and surface modification (SM). In the absence of phage or at a low force of infection, CRISPRs are favored over SM, since the latter is associated with a fixed cost of resistance. At high phage exposure, SM is favored over the CRISPR, because the latter is associated with an inducible cost of resistance that increases with an increasing force of infection. Empirical support for this was reported previously (133).

FIG 4

Although empirical support is currently lacking, it may be the case that increasing phage diversity can select for broad-range innate immune mechanisms, such as RM, over specific adaptive immune systems, such as the CRISPR-Cas system. While the CRISPR system is extremely effective if there is low genetic variation in the phage population, theory predicts that the system becomes less effective if the host is exposed to a phage population with high levels of genetic diversity (149).

FIG 5

Mutualists (e.g., plasmids that confer a fitness benefit to the bacterial host) can select against immune mechanisms (177). If both mutualists and parasites are present (e.g., plasmid and phage [left] or beneficial and harmful plasmids [right]), CRISPRs and pAgo may be beneficial since their specificity allows bacterial hosts to specifically acquire resistance against the parasite. Empirical data to support this idea are currently lacking.

FIG 6

Spatial structure is an important fitness determinant for Abi, since it impacts relatedness. In the absence of phage, there will be selection against Abi because of the cost of carrying the system. In a structured environment, the benefits of Abi are directed toward related individuals that also carry the Abi gene. The phage will die out rapidly in the presence of Abi, while the phage will cause an epidemic in the absence of Abi (progeny phage is indicated in gray). In a well-mixed environment, bacteria lacking the Abi system benefit from the altruistic defense of bacteria that encode the Abi system, but they do not pay the cost. Both strains equally suffer from the epidemic that results from infection of bacteria that lack the Abi system. Empirical support for these findings was reported previously (181–183).