Multi-omics landscape and molecular basis of radiation tolerance in a tardigrade

Lei Li, Zhengping Ge, Shihao Liu, Kun Zheng, Yaqi Li, Kaiqi Chen, Yesheng Fu, Xiaoguang Lei, Zeling Cui, Yifan Wang, Jin Huang, Yanyan Liu, Mingwang Duan, Zimei Sun, Jun Chen, Liangwei Li, Pan Shen, Guibin Wang, Junmiao Chen, Ruochong Li, Chaoran Li, Zhixiang Yang, Yifan Ning, Arong Luo, Baoyu Chen, Inge Seim, Xin Liu, Fei Wang, Yishan Yao, Fusheng Guo, Maojun Yang, Cui Hua Liu, Guangyi Fan, Lizhi Wang, Dong Yang, Lingqiang Zhang.

Science, 25 Oct 2024
Vol 386, Issue 6720
DOI: 10.1126/science.adl0799

Tardigrades are captivating organisms known for their resilience in extreme environments, including ultra-high-dose radiation, but the underlying mechanisms of this resilience remain largely unknown. Using genome, transcriptome, and proteome analysis of Hypsibius henanensis sp. nov., we explored the molecular basis contributing to radiotolerance in this organism. A putatively horizontally transferred gene, DOPA dioxygenase 1 (DODA1), responds to radiation and confers radiotolerance by synthesizing betalain —a type of plant pigment with free radical-scavenging properties. A tardigrade-specific radiation-induced disordered protein, TRID1, facilitates DNA damage repair through a mechanism involving phase separation. Two mitochondrial respiratory chain complex assembly proteins, BCS1 and NDUFB8, accumulate to accelerate nicotinamide adenine dinucleotide (NAD+) regeneration for poly (adenosine diphosphate–ribosyl)ation (PARylation) and subsequent poly(adenosine diphosphate–ribose) polymerase 1 (PARP1)–mediated DNA damage repair. These three observations expand our understanding of mechanisms of tardigrade radiotolerance.