Telomeres of Oxytricha macronuclear chromatin exist as discrete nonnucleosomal DNA-protein complexes, each of which encompasses the terminal 100-150 bp of a macronuclear DNA molecule. We have used chemical and nuclease footprinting to examine the internal structure of these telomeric complexes. Remarkably salt-stable DNA-protein interactions result in methylation-protection of specific guanine residues in the 3'-terminal T4G4T4G4 tail. The methylation pattern seen in vivo and in isolated macronuclei is reconstituted in vitro when purified 55-kD and 43-kD telomere proteins are added to purified macronuclear DNA. Very different interactions are observed between protein and DNA within the region approximately 45-135 bp from the 5' terminus. The DNase I cleavage pattern indicates that this DNA lies on the outside surface of protein but is not part of a nucleosome. Our data suggest that the telomeric complexes have two structural domains characterized by their dissimilar DNA-protein interactions. We propose that functionally equivalent telomeres from other organisms could be accommodated in a similar telomeric chromatin structure.