Mixed mode transmission of phages drives loss of Type I CRISPR-Cas immune systems from bacteria

Upon infection of their host, temperate phages (viruses that infect bacteria) enter either the lytic or the lysogenic cycle, causing host lysis and horizontal transmission or dormancy and vertical transmission, respectively. Co-culture experiments of bacteria and obligately killing temperate phage mutants - that are locked in the lytic cycle - have provided key insights into the evolutionary dynamics of CRISPR-Cas and phage interactions, but ignore this dichotomy of temperate phage transmission strategies. Here we show that type I CRISPR-Cas immune systems are much less efficient in clearing wildtype temperate phage infections from the bacterial population than phage mutants locked in the lytic cycle, and are in fact maladaptive to the host due to severe immunopathological effects that specifically manifest during vertical transmission of the phage. These fitness costs drive the loss of CRISPR-Cas from bacterial populations, unless the phage carries anti-CRISPR (acr) genes that suppress the immune system of the host. The opposing fitness consequences of CRISPR-Cas in the face of horizontally and vertically transmitting phages can therefore help to explain the frequent loss and gain of CRISPR-Cas immune systems across bacterial strains, and highlight the strong selective benefits of phage-encoded acr genes during long-lived infections associated with vertical transmission.