TY - JOUR
T1 - Common and unique strategies of myoglobin evolution for deep-sea adaptation of diving mammals
AU - Isogai, Yasuhiro
AU - Imamura, Hiroshi
AU - Nakae, Setsu
AU - Sumi, Tomonari
AU - Takahashi, Ken ichi
AU - Shirai, Tsuyoshi
N1 - Funding Information:
We thank Satoshi Kawasaki (https://paleontology.sakura.ne.jp/) for the kind permission to use his illustrations of animals. X-ray diffraction and SAXS experiments were conducted at SPring-8 and KEK, Japan, respectively, under the approval of the Photon Factory Program Advisory Committee: Proposal No. 2018G032 and No. 2020G077. This work was partly supported by Grants-in-Aid for scientific research from the Ministry of Education, Culture, Sports, Science and Technology-Japan (JP17H01818, JP21K06503 and JP21H03547) and the Platform Project for Supporting Drug Discovery and Life Science Research (Basis of Supporting Innovative Drug Discovery and Life Science Research (BINDS)) from AMED (JP20am0101111j0004 support number 0792). Y.I. and T. Shirai designed the research. K.T. and T. Shirai predicted the ancestral protein sequences. Y.I. synthesized proteins and performed biochemical analyses. S.N. and T. Shirai performed protein crystallization and 3D structure determination. Y.I. T. Sumi, K.T. and T. Shirai conducted theoretical calculations. H.I. and Y.I. performed SAXS measurements and analyses. Y.I. and T. Shirai wrote the main manuscript text. All authors reviewed the manuscript. The authors declare that they have no financial and/or nonfinancial competing interests with the contents of this article.
Funding Information:
We thank Satoshi Kawasaki ( https://paleontology.sakura.ne.jp/ ) for the kind permission to use his illustrations of animals. X-ray diffraction and SAXS experiments were conducted at SPring-8 and KEK, Japan, respectively, under the approval of the Photon Factory Program Advisory Committee: Proposal No. 2018G032 and No. 2020G077. This work was partly supported by Grants-in-Aid for scientific research from the Ministry of Education, Culture, Sports, Science and Technology -Japan ( JP17H01818 , JP21K06503 and JP21H03547 ) and the Platform Project for Supporting Drug Discovery and Life Science Research (Basis of Supporting Innovative Drug Discovery and Life Science Research (BINDS)) from AMED ( JP20am0101111j0004 support number 0792).
Publisher Copyright:
© 2021 The Author(s)
PY - 2021/8/20
Y1 - 2021/8/20
N2 - Myoglobin (Mb) is highly concentrated in the myocytes of diving mammals such as whales and seals, in comparison with land animals, and its molecular evolution has played a crucial role in their deep-sea adaptation. We previously resurrected ancestral whale Mbs and demonstrated the evolutional strategies for higher solubility under macromolecular crowding conditions. Pinnipeds, such as seals and sea lions, are also expert diving mammals with Mb-rich muscles. In the present study, we resurrected ancestral pinniped Mbs and investigated their biochemical and structural properties. Comparisons between pinniped and whale Mbs revealed the common and distinctive strategies for the deep-sea adaptation. The overall evolution processes, gaining precipitant tolerance and improving thermodynamic stability, were commonly observed. However, the strategies for improving the folding stability differed, and the pinniped Mbs exploited the shielding of hydrophobic surfaces more effectively than the whale Mbs.
AB - Myoglobin (Mb) is highly concentrated in the myocytes of diving mammals such as whales and seals, in comparison with land animals, and its molecular evolution has played a crucial role in their deep-sea adaptation. We previously resurrected ancestral whale Mbs and demonstrated the evolutional strategies for higher solubility under macromolecular crowding conditions. Pinnipeds, such as seals and sea lions, are also expert diving mammals with Mb-rich muscles. In the present study, we resurrected ancestral pinniped Mbs and investigated their biochemical and structural properties. Comparisons between pinniped and whale Mbs revealed the common and distinctive strategies for the deep-sea adaptation. The overall evolution processes, gaining precipitant tolerance and improving thermodynamic stability, were commonly observed. However, the strategies for improving the folding stability differed, and the pinniped Mbs exploited the shielding of hydrophobic surfaces more effectively than the whale Mbs.
KW - Biomolecules
KW - Evolutionary biology
KW - Evolutionary mechanisms
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U2 - 10.1016/j.isci.2021.102920
DO - 10.1016/j.isci.2021.102920
M3 - Article
AN - SCOPUS:85112373020
SN - 2589-0042
VL - 24
JO - iScience
JF - iScience
IS - 8
M1 - 102920
ER -