4.7 Article

Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors

Journal

MOLECULAR ECOLOGY RESOURCES
Volume 19, Issue 5, Pages 1292-1308

Publisher

WILEY
DOI: 10.1111/1755-0998.13023

Keywords

ciliated protist; environmental stress; frameshifting; genome rearrangement

Funding

  1. Div Of Molecular and Cellular Bioscience
  2. Direct For Biological Sciences [1158346] Funding Source: National Science Foundation
  3. Fundamental Research Funds for the Central Universities [201841013, 201762017] Funding Source: Medline
  4. National Natural Science Foundation of China [31772428] Funding Source: Medline
  5. National Science Foundation [DEB-1541511, 1158346] Funding Source: Medline
  6. NIGMS NIH HHS [R15 GM113177] Funding Source: Medline
  7. NIH HHS [P40 OD010964, P40OD010964, 1R15GM113177-01] Funding Source: Medline
  8. Young Elite Scientists Sponsorship Program by CAST [2017QNRC001] Funding Source: Medline
  9. Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) [2018SDKJ0406-1] Funding Source: Medline

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As a model organism for studies of cell and environmental biology, the free-living and cosmopolitan ciliate Euplotes vannus shows intriguing features like dual genome architecture (i.e., separate germline and somatic nuclei in each cell/organism), gene-sized chromosomes, stop codon reassignment, programmed ribosomal frameshifting (PRF) and strong resistance to environmental stressors. However, the molecular mechanisms that account for these remarkable traits remain largely unknown. Here we report a combined analysis of de novo assembled high-quality macronuclear (MAC; i.e., somatic) and partial micronuclear (MIC; i.e., germline) genome sequences for E. vannus, and transcriptome profiling data under varying conditions. The results demonstrate that: (a) the MAC genome contains more than 25,000 complete gene-sized nanochromosomes (~85 Mb haploid genome size) with the N50 ~2.7 kb; (b) although there is a high frequency of frameshifting at stop codons UAA and UAG, we did not observe impaired transcript abundance as a result of PRF in this species as has been reported for other euplotids; (c) the sequence motif 5 '-TA-3 ' is conserved at nearly all internally-eliminated sequence (IES) boundaries in the MIC genome, and chromosome breakage sites (CBSs) are duplicated and retained in the MAC genome; (d) by profiling the weighted correlation network of genes in the MAC under different environmental stressors, including nutrient scarcity, extreme temperature, salinity and the presence of ammonia, we identified gene clusters that respond to these external physical or chemical stimulations, and (e) we observed a dramatic increase in HSP70 gene transcription under salinity and chemical stresses but surprisingly, not under temperature changes; we link this temperature-resistance to the evolved loss of temperature stress-sensitive elements in regulatory regions. Together with the genome resources generated in this study, which are available online at Euplotes vannus Genome Database (), these data provide molecular evidence for understanding the unique biology of highly adaptable microorganisms.

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