Increased genetic diversity loss and genetic differentiation in a model marine diatom adapted to ocean warming compared to high CO.

Peng Jin, Jiaofeng Wan, Yunyue Zhou, Kunshan Gao, John Beardall, Jiamin Lin, Jiali Huang, Yucong Lu, Shiman Liang, Kaiqiang Wang, Zengling Ma, Jianrong Xia
Author Information
  1. Peng Jin: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China.
  2. Jiaofeng Wan: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China.
  3. Yunyue Zhou: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China.
  4. Kunshan Gao: State Key Laboratory of Marine Environmental Science & College of Ocean and Earth Sciences, Xiamen University, 361005, Xiamen, China. ORCID
  5. John Beardall: State Key Laboratory of Marine Environmental Science & College of Ocean and Earth Sciences, Xiamen University, 361005, Xiamen, China. ORCID
  6. Jiamin Lin: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China.
  7. Jiali Huang: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China.
  8. Yucong Lu: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China.
  9. Shiman Liang: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China.
  10. Kaiqiang Wang: Gene Denovo Biotechnology Co, Guangzhou, 510006, China.
  11. Zengling Ma: Zhejiang Provincial Key Laboratory for Subtropical Water Environment and Marine Biological Resources Protection, Wenzhou University, Wenzhou, 325035, China. ORCID
  12. Jianrong Xia: School of Environmental Science and Engineering, Guangzhou University, Guangzhou, 510006, China. jrxia@gzhu.edu.cn. ORCID

Abstract

Although high CO and warming could act interactively on marine phytoplankton, little is known about the molecular basis for this interaction on an evolutionary scale. Here we explored the adaptation to high CO in combination with warming in a model marine diatom Phaeodactylum tricornutum. Whole-genome re-sequencing identifies, in comparison to populations grown under control conditions, a larger genetic diversity loss and a higher genetic differentiation in the populations adapted for 2 years to warming than in those adapted to high CO. However, this diversity loss was less under high CO combined with warming, suggesting that the evolution driven by warming was constrained by high CO. By integrating genomics, transcriptomics, and physiological data, we found that the underlying molecular basis for this constraint is associated with the expression of genes involved in some key metabolic pathways or biological processes, such as the glyoxylate pathway, amino acid and fatty acid metabolism, and diel variability. Our results shed new light on the evolutionary responses of marine phytoplankton to multiple environmental changes in the context of global change and provide new insights into the molecular basis underpinning interactions among those multiple drivers.

References

  1. Bioinformatics. 2009 Jul 15;25(14):1754-60 [PMID: 19451168]
  2. Nat Commun. 2018 Apr 30;9(1):1719 [PMID: 29712900]
  3. Genome Biol. 2014;15(12):550 [PMID: 25516281]
  4. Bioinformatics. 2018 Sep 1;34(17):i884-i890 [PMID: 30423086]
  5. Nucleic Acids Res. 2010 Sep;38(16):e164 [PMID: 20601685]
  6. Sci Total Environ. 2021 Jun 1;771:145167 [PMID: 33736151]
  7. Proc Natl Acad Sci U S A. 2015 Oct 27;112(43):13272-7 [PMID: 26460052]
  8. Nature. 2008 Nov 13;456(7219):239-44 [PMID: 18923393]
  9. Evolution. 2013 Jul;67(7):1869-78 [PMID: 23815645]
  10. Proc Natl Acad Sci U S A. 2013 Jun 11;110(24):9824-9 [PMID: 23703908]
  11. Ecol Lett. 2016 Feb;19(2):133-142 [PMID: 26610058]
  12. Proc Natl Acad Sci U S A. 2019 Feb 5;116(6):2152-2157 [PMID: 30659151]
  13. Nat Protoc. 2016 Sep;11(9):1650-67 [PMID: 27560171]
  14. PLoS One. 2013 May 21;8(5):e63091 [PMID: 23704890]
  15. Science. 2012 Nov 23;338(6110):1085-8 [PMID: 23112294]
  16. Evol Appl. 2016 Feb 28;9(9):1156-1164 [PMID: 27695523]
  17. Nat Commun. 2015 Sep 01;6:8155 [PMID: 26327191]
  18. Genome Biol. 2010;11(2):R17 [PMID: 20146805]
  19. Can J Microbiol. 1962 Apr;8:229-39 [PMID: 13902807]
  20. Nature. 2016 Jun 01;534(7605):102-5 [PMID: 27251284]
  21. ISME J. 2020 Feb;14(2):347-363 [PMID: 31624346]
  22. Nat Rev Genet. 2003 Jun;4(6):457-69 [PMID: 12776215]
  23. Funct Plant Biol. 2003 Feb;30(2):171-186 [PMID: 32689003]
  24. Nature. 2009 May 14;459(7244):185-92 [PMID: 19444204]
  25. Microbiol Mol Biol Rev. 2018 Jul 25;82(3): [PMID: 30045954]
  26. Nat Biotechnol. 2015 Mar;33(3):290-5 [PMID: 25690850]
  27. Mar Environ Res. 2020 Feb;154:104871 [PMID: 31928985]
  28. Science. 2008 May 23;320(5879):1034-9 [PMID: 18497287]
  29. Science. 2015 Jul 3;349(6243):aac4722 [PMID: 26138982]
  30. Science. 1998 Jul 10;281(5374):237-40 [PMID: 9657713]
  31. Science. 2009 Aug 28;325(5944):1095-8 [PMID: 19713521]
  32. Ecol Lett. 2020 Apr;23(4):722-733 [PMID: 32059265]
  33. Glob Chang Biol. 2018 Jun;24(6):2239-2261 [PMID: 29476630]
  34. Nat Methods. 2012 Mar 04;9(4):357-9 [PMID: 22388286]
  35. Nat Commun. 2020 Feb 20;11(1):971 [PMID: 32080175]
  36. Proc Natl Acad Sci U S A. 2017 Sep 12;114(37):9930-9935 [PMID: 28847969]
  37. Nat Methods. 2015 Apr;12(4):357-60 [PMID: 25751142]
  38. Ann Rev Mar Sci. 2020 Jan 3;12:181-208 [PMID: 31451085]
  39. Plant Physiol. 2012 Jan;158(1):499-513 [PMID: 22095044]
  40. Science. 2017 Dec 1;358(6367):1149-1154 [PMID: 29191900]
  41. Nat Plants. 2020 Aug;6(8):1031-1043 [PMID: 32719473]
  42. Photosynth Res. 2011 Sep;109(1-3):191-203 [PMID: 21287273]
  43. Heredity (Edinb). 2008 May;100(5):464-70 [PMID: 18212804]
  44. Nat Commun. 2019 Dec 20;10(1):5821 [PMID: 31862880]
  45. Nat Commun. 2021 Sep 10;12(1):5372 [PMID: 34508102]
  46. Sci Rep. 2018 Dec 11;8(1):17771 [PMID: 30538260]
  47. New Phytol. 2022 Mar;233(5):2155-2167 [PMID: 34907539]

MeSH Term

Amino Acids
Carbon Dioxide
Diatoms
Fatty Acids
Genetic Variation
Glyoxylates
Oceans and Seas
Phytoplankton

Chemicals

Amino Acids
Fatty Acids
Glyoxylates
Carbon Dioxide

Word Cloud

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