Pressure tolerance of deep-sea enzymes can be evolved through increasing volume changes in protein transitions: a study with lactate dehydrogenases from abyssal and hadal fishes

Mackenzie E. Gerringer, Paul H. Yancey, Olga V. Tikhonova, Nikita E. Vavilov, Victor G. Zgoda, Dmitri R. Davydov

Research output: Contribution to journalArticlepeer-review

9 Scopus citations

Abstract

We explore the principles of pressure tolerance in enzymes of deep-sea fishes using lactate dehydrogenases (LDH) as a case study. We compared the effects of pressure on the activities of LDH from hadal snailfishes Notoliparis kermadecensis and Pseudoliparis swirei with those from a shallow-adapted Liparis florae and an abyssal grenadier Coryphaenoides armatus. We then quantified the LDH content in muscle homogenates using mass-spectrometric determination of the LDH-specific conserved peptide LNLVQR. Existing theory suggests that adaptation to high pressure requires a decrease in volume changes in enzymatic catalysis. Accordingly, evolved pressure tolerance must be accompanied with an important reduction in the volume change associated with pressure-promoted alteration of enzymatic activity ((Formula presented.) ). Our results suggest an important revision to this paradigm. Here, we describe an opposite effect of pressure adaptation—a substantial increase in the absolute value of (Formula presented.) in deep-living species compared to shallow-water counterparts. With this change, the enzyme activities in abyssal and hadal species do not substantially decrease their activity with pressure increasing up to 1–2 kbar, well beyond full-ocean depth pressures. In contrast, the activity of the enzyme from the tidepool snailfish, L. florae, decreases nearly linearly from 1 to 2500 bar. The increased tolerance of LDH activity to pressure comes at the expense of decreased catalytic efficiency, which is compensated with increased enzyme contents in high-pressure-adapted species. The newly discovered strategy is presumably used when the enzyme mechanism involves the formation of potentially unstable excited transient states associated with substantial changes in enzyme–solvent interactions.
Original languageEnglish (US)
Pages (from-to)5394-5410
Number of pages17
JournalFEBS Journal
Volume287
Issue number24
DOIs
StatePublished - Apr 6 2020
Externally publishedYes

Bibliographical note

KAUST Repository Item: Exported on 2022-06-14
Acknowledgements: The authors thank Doug Bartlett (UCSD) and Jeff Jones (WSU) for opening their laboratories to this work and Jeffrey Drazen (University of Hawaiʻi) and Logan Peoples (UCSD) for research support. We are grateful for Thomas Linley (Newcastle University), Alan Jamieson (Newcastle University), Matteo Ichino (University of Southampton), Chloe Weinstock (Whitman College), and the science parties of the National Science Foundation (NSF) and Schmidt Ocean Institute’s (SOI) HADES Program cruises, who assisted with collection and processing of fish samples at sea. Thanks to Matt Tietbohl (KAUST), Stacy Farina (Howard University), and Adam Summers (Friday Harbor Labs) for their contributions to L. florae collection and dissection. The authors thank the captains and crews of the R/Vs Thompson, R/V Centennial, and R/V Falkor. Authors are also grateful to the ‘Human Proteome’ Core Facility, Institute of Biomedical Chemistry (IBMC), which is supported by the Ministry of Education and Science of the Russian Federation (agreement 14.621.21.0017, unique project ID RFMEFI62117X0017). This research was supported by the grants from National Science Foundation (NSF-OCE 1130494 to P. Yancey and 1130712 and 1508760 to J. Drazen covering M. Gerringer’s work) and Schmidt Ocean Institute (FK141109 to J. Drazen and P. Yancey). M. Gerringer is grateful for the support of the National Science Foundation’s Graduate Research Fellowships Program, the Seaver Institute, and the State University of New York at Geneseo. Mass-spectrometric part of this work was done within the framework of the Russian State Academy of Sciences Fundamental Scientific Research Program for 2013–2020. The funding sources had no involvement in the study design, collection, analysis, and interpretation of data, as well as in the decision to submit the article for publication.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

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