CrAssphage is the most abundant human-associated virus and the founding member 
of a large group of bacteriophages, discovered in animal-associated and 
environmental metagenomes, that infect bacteria of the phylum Bacteroidetes. We 
analyze 4907 Circular Metagenome Assembled Genomes (cMAGs) of putative viruses 
from human gut microbiomes and identify nearly 600 genomes of crAss-like phages 
that account for nearly 87% of the DNA reads mapped to these cMAGs. Phylogenetic 
analysis of conserved genes demonstrates the monophyly of crAss-like phages, a 
putative virus order, and of 5 branches, potential families within that order, 
two of which have not been identified previously. The phage genomes in one of 
these families are almost twofold larger than the crAssphage genome (145-192 
kilobases), with high density of self-splicing introns and inteins. Many 
crAss-like phages encode suppressor tRNAs that enable read-through of UGA or UAG 
stop-codons, mostly, in late phage genes. A distinct feature of the crAss-like 
phages is the recurrent switch of the phage DNA polymerase type between A and B 
families. Thus, comparative genomic analysis of the expanded assemblage of 
crAss-like phages reveals aspects of genome architecture and expression as well 
as phage biology that were not apparent from the previous work on phage 
genomics.