Evolutionary Ecology of Prokaryotic Immune Mechanisms
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crossmark Evolutionary Ecology of Prokaryotic Immune Mechanisms Stineke van Houte, Angus Buckling, Edze R. Westra ESI and CEC, Department of Biosciences, University of Exeter, Exeter, United Kingdom SUMMARY ..................................................................................................................................................745 INTRODUCTION ............................................................................................................................................745 Downloaded from DIFFERENT RESISTANCE MECHANISMS OF BACTERIA ....................................................................................................746 Surface Modification .....................................................................................................................................746 Superinfection Exclusion .................................................................................................................................746 Restriction-Modification ..................................................................................................................................747 CRISPR-Cas Systems ......................................................................................................................................747 Class 1 CRISPR-Cas systems ............................................................................................................................747 Class 2 CRISPR-Cas systems ............................................................................................................................748 pAgo .....................................................................................................................................................748 Abortive Infection ........................................................................................................................................748 SELECTIVE FORCES DRIVING THE EVOLUTION OF IMMUNE MECHANISMS ..............................................................................749 http://mmbr.asm.org/ Is More Immunity Best?...................................................................................................................................749 Fitness Costs of Immunity ................................................................................................................................749 Surface modification...................................................................................................................................749 Superinfection exclusion ..............................................................................................................................749 Restriction-modification ...............................................................................................................................749 CRISPR-Cas.............................................................................................................................................749 Abortive infection......................................................................................................................................750 Costs of Resistance Can Help To Explain Diversity in Immune Mechanisms..............................................................................750 How Does Symbiont Diversity Contribute to Immune Diversity? ........................................................................................750 Diverse pathogens: intraspecific diversity .............................................................................................................751 Diverse pathogens: interspecific diversity .............................................................................................................752 Mutualists..............................................................................................................................................752 on July 25, 2016 by UNIVERSITY OF EXETER Impact of Spatial Structure on Evolution of Immune Mechanisms .......................................................................................752 CONSEQUENCES OF OPERATION OF DIFFERENT MECHANISMS..........................................................................................753 Coevolution with Different Immune Mechanisms .......................................................................................................753 Surface modification...................................................................................................................................753 Superinfection exclusion ..............................................................................................................................754 Restriction-modification ...............................................................................................................................754 CRISPR-Cas.............................................................................................................................................755 Abortive infection......................................................................................................................................755 Broader Consequences of Different Immune Mechanisms...............................................................................................755 Alternative Function of Immune Mechanisms ...........................................................................................................756 APPLICATIONS, CONCLUSIONS, AND OUTLOOK ..........................................................................................................756 ACKNOWLEDGMENTS......................................................................................................................................756 REFERENCES ................................................................................................................................................757 SUMMARY nome replication. First, immunity by surface modification results Bacteria have a range of distinct immune strategies that provide pro- from masking, mutation, or loss of host receptor proteins, which tection against bacteriophage (phage) infections. While much has serve as entry points for the phage. Second, the host can block been learned about the mechanism of action of these defense strate- phage DNA injection or phage replication, known as superinfec- gies, it is less clear why such diversity in defense strategies has evolved. tion exclusion (Sie). Third, injected phage genomes can be cleaved In this review, we discuss the short- and long-term costs and benefits by at least three distinct intracellular immune mechanisms: re- of the different resistance strategies and, hence, the ecological condi- striction-modification (RM), the CRISPR-Cas (clustered regu- tions that are likely to favor the different strategies alone and in com- larly interspaced short palindromic repeat–CRISPR-associated bination. Finally, we discuss some of the broader consequences, be- gene) system, and prokaryotic Argonaute (pAgo). Finally, bacteria yond resistance to phage and other genetic elements, resulting from the operation of different immune strategies. INTRODUCTION Published 13 July 2016 Citation van Houte S, Buckling A, Westra ER. 2016. Evolutionary ecology of acteria are under constant threat by viruses (bacteriophages prokaryotic immune mechanisms. Microbiol Mol Biol Rev 80:745–763. B[phages]) and have evolved multiple immune strategies to doi:10.1128/MMBR.00011-16. combat phage infections (Fig. 1). Phage immune mechanisms can Address correspondence to Edze R. Westra, [email protected]. act at different stages of the phage life cycle, including receptor Copyright © 2016, American Society for Microbiology. All Rights Reserved. binding, genome injection into the host cell, and intracellular ge- September 2016 Volume 80 Number 3 Microbiology and Molecular Biology Reviews mmbr.asm.org 745 van Houte et al. Downloaded from 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). http://mmbr.asm.org/ can trigger a suicide reaction upon phage infection, known as study on the fish pathogen Vibrio anguillarum and its phage, abortive infection (Abi), resulting in infection failure. The molec- KVP40, showed that quorum sensing is used by bacteria to alter- ular mechanism of these immune strategies has been the subject of nate between two different phage protection mechanisms. At several excellent reviews (see references 1–3) and are reiterated low population densities, Vibrio shows high-level expression of below. Below, we discuss how ecological selection pressures have OmpK, the main receptor for phage KVP40, but is protected driven the evolution of diverse bacterial immune mechanisms and against phage infection by increased biofilm formation. As popu- the broader ecological and evolutionary consequences of their ex- lation densities increase, however, OmpK expression is down- istence beyond resistance to viruses and other mobile genetic ele- regulated through quorum sensing regulation, which renders ments. In this review, we use the terms resistance, defense, and Vibrio almost fully resistant to the phage (9). immunity interchangeably. Where receptor loss is too costly, receptor mutation, blocking, on July 25, 2016 by UNIVERSITY OF EXETER or masking may be favored by selection. Evidence for frequent