This study demonstrates that the chromosome of the hyperthermophilic archaeon Thermococcus kodakarensis is organized into a heterogeneous structure created with histone and a novel protein TK0471/TrmBL2. TK0471/TrmBL2 plays dual roles as a chromosomal protein and as a global transcriptional repressor, and it is conserved in some archaeal and bacterial species.

We have applied chromatin sequencing technology to the euryarchaeon Thermococcus kodakarensis, which is known to possess histone-like proteins. We detect positioned chromatin particles of variable sizes associated with lengths of DNA differing as multiples of 30 bp (ranging from 30 bp to 4450 bp) consistent with formation from dynamic polymers of the archaeal histone dimer. T. kodakarensis chromatin particles have distinctive underlying DNA sequence suggesting a genomic particle-positioning code and are excluded from gene-regulatory DNA suggesting a functional organization. Beads-on-a-string chromatin is therefore conserved between eukaryotes and archaea but can derive from deployment of histone-fold proteins in a variety of multimeric forms.

The nematode Caenorhabditis elegans, after completing its developmental stages and a brief reproductive period, spends the remainder of its adult life as an organism consisting exclusively of post-mitotic cells. Here we show that telomere length varies considerably in clonal populations of wild-type worms, and that these length differences are conserved over at least ten generations, suggesting a length regulation mechanism in cis. This observation is strengthened by the finding that the bulk telomere length in different worm strains varies considerably. Despite the close correlation of telomere length and clonal cellular senescence in mammalian cells, nematodes with long telomeres were neither long lived, nor did worm populations with comparably short telomeres exhibit a shorter life span. Conversely, long-lived daf-2 and short-lived daf-16 mutant animals can have either long or short telomeres. Telomere length of post-mitotic cells did not change during the aging process, and the response of animals to stress was found independent of telomere length. Collectively, our data indicate that telomere length and life span can be uncoupled in a post-mitotic setting, suggesting separate pathways for replication-dependent and -independent aging.

Background: TrmBL2 and histones maintain the genome functioning in hyperthermophilic euryarchaeal cells. Results: TrmBL2 forms filaments on DNA through cooperative binding and competes with histones in a salt-and DNA supercoiling-dependent manner. Conclusion: TrmBL2-histone collective behavior dynamically controls DNA organization. Significance: The discovered mechanisms provide insights into the regulation of the genome structure and global transcription profile by TrmBL2 and histones.