Common and unique strategies of myoglobin evolution for deep-sea adaptation of diving mammals

Yasuhiro Isogai; Hiroshi Imamura; Setsu Nakae; Tomonari Sumi; Ken-Ichi Takahashi; Tsuyoshi Shirai

doi:10.1016/j.isci.2021.102920

Common and unique strategies of myoglobin evolution for deep-sea adaptation of diving mammals

iScience. 2021 Jul 30;24(8):102920. doi: 10.1016/j.isci.2021.102920. eCollection 2021 Aug 20.

Authors

Yasuhiro Isogai¹, Hiroshi Imamura², Setsu Nakae³, Tomonari Sumi⁴, Ken-Ichi Takahashi³, Tsuyoshi Shirai³

Affiliations

¹ Department of Pharmaceutical Engineering, Toyama Prefectural University, Imizu, Toyama 939-0398, Japan.
² Department of Applied Chemistry, College of Life Sciences, Ritsumeikan University, 1-1-1 Nojihigashi, Kusatsu, Shiga 525-8577, Japan.
³ Department of Computer Bioscience, Nagahama Institute of Bio-Science and Technology, 1266 Tamura-Cho, Nagahama, Shiga 526-0829, Japan.
⁴ Research Institute for Interdisciplinary Science, Okayama University, 3-1-1 Tsushima-Naka, Kita-ku, Okayama 700-8530, Japan.

Abstract

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.

Keywords: Biomolecules; Evolutionary biology; Evolutionary mechanisms.