Crenarchaea is a phyla in the archaeal domain. Unlike the well-characterized DNA folding dynamics of histone-containing euryarchaea, the crenarchaeal mechanism of chromatin compaction and its control still remains unclear. To gain insight on the folding dynamics of the crenarchaeal genome, its chromatin structure was investigated at different growth phases. MNase digestion revealed that crenarchaeal chromatin do not have regularly repeating nucleoprotein units in their genome unlike histone-containing euryarchaea. Also, morphological analysis of their nucleoid showed that majority of the cells have compact nucleoid regions during log phase that relax as they transition to stationary phase. On-substrate lysis and atomic force microscopy revealed beaded fiber structures as the primary structure of crenarchaeal chromatin, similar to those found in histone-containing archaea. Chromatin binding proteins were profiled and putative architectural proteins were identified. These results suggest that although crenarchaea employ chromatin architectural proteins other than histones to regulate chromatin folding, they may have similar folding mechanisms with histone-containing euryarchaea, as evidenced by similarities in their basic chromatin structural unit. Additionally, increased chromatin compaction may imply a highly organized genomic architecture during log phase while decompaction of chromatin during stationary phase may be due to a less transcriptionally active chromatin.