Selection for Late Reproduction Leads to Loss of Complex I Mitochondrial Capacity and Associated Increased Longevity in Seed Beetles

Overview

Journal J Gerontol A Biol Sci Med Sci

Specialty Geriatrics

Date 2024 Aug 19

PMID 39158488

Authors

Heather E Mast

Pierre U Blier

Mirko ordevic

Uros Savkovic

Claudia D Holody

Stephane L Bourque

Helene Lemieux

Affiliations

Soon will be listed here.

Abstract

Mitochondria play a key role in aging. Here, we measured integrated mitochondrial functions in experimentally evolved lines of the seed beetle Acanthoscelides obtectus that were selected for early (E) or late (L) reproduction for nearly 4 decades. The 2 lines have markedly different lifespans (8 days and 13 days in the E and L lines, respectively). The contribution of the NADH pathway to maximal flux was lower in the L compared to the E beetles at young stages, associated with increased control by complex I. In contrast, the contribution of the Succinate pathway was higher in the L than in the E line, whereas the Proline pathway showed no differences between the lines. Our data suggest that selection of age at reproduction leads to a modulation of complex I activity in mitochondria and that mitochondria are a functional link between evolutionary and mechanistic theories of aging.

References

Larsen S, Nielsen J, Hansen C, Nielsen L, Wibrand F, Stride N . Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol. 2012; 590(14):3349-60. PMC: 3459047. DOI: 10.1113/jphysiol.2012.230185. View

Lopez-Otin C, Blasco M, Partridge L, Serrano M, Kroemer G . The hallmarks of aging. Cell. 2013; 153(6):1194-217. PMC: 3836174. DOI: 10.1016/j.cell.2013.05.039. View

Curran S, Ruvkun G . Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 2007; 3(4):e56. PMC: 1847696. DOI: 10.1371/journal.pgen.0030056. View

Mukai Y, Kamei Y, Liu X, Jiang S, Sugimoto Y, Mat Nanyan N . Proline metabolism regulates replicative lifespan in the yeast . Microb Cell. 2019; 6(10):482-490. PMC: 6780008. DOI: 10.15698/mic2019.10.694. View

Baumgart M, Priebe S, Groth M, Hartmann N, Menzel U, Pandolfini L . Longitudinal RNA-Seq Analysis of Vertebrate Aging Identifies Mitochondrial Complex I as a Small-Molecule-Sensitive Modifier of Lifespan. Cell Syst. 2016; 2(2):122-32. DOI: 10.1016/j.cels.2016.01.014. View

Loeffen J, Smeitink J, Trijbels J, Janssen A, Triepels R, Sengers R . Isolated complex I deficiency in children: clinical, biochemical and genetic aspects. Hum Mutat. 2000; 15(2):123-34. DOI: 10.1002/(SICI)1098-1004(200002)15:2<123::AID-HUMU1>3.0.CO;2-P. View

Darveau C, Hochachka P, Roubik D, Suarez R . Allometric scaling of flight energetics in orchid bees: evolution of flux capacities and flux rates. J Exp Biol. 2005; 208(Pt 18):3593-602. DOI: 10.1242/jeb.01777. View

Hansen M, Hsu A, Dillin A, Kenyon C . New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet. 2005; 1(1):119-28. PMC: 1183531. DOI: 10.1371/journal.pgen.0010017. View

Pang S, Curran S . Adaptive capacity to bacterial diet modulates aging in C. elegans. Cell Metab. 2014; 19(2):221-31. PMC: 3979424. DOI: 10.1016/j.cmet.2013.12.005. View

10.

Immonen E, Sayadi A, Stojkovic B, Savkovic U, dordevic M, Liljestrand-Ronn J . Experimental Life History Evolution Results in Sex-specific Evolution of Gene Expression in Seed Beetles. Genome Biol Evol. 2022; 15(1). PMC: 9830990. DOI: 10.1093/gbe/evac177. View

11.

Hamilton B, Dong Y, Shindo M, Liu W, Odell I, Ruvkun G . A systematic RNAi screen for longevity genes in C. elegans. Genes Dev. 2005; 19(13):1544-55. PMC: 1172061. DOI: 10.1101/gad.1308205. View

12.

dordevic M, Stojkovic B, Savkovic U, Immonen E, Tucic N, Lazarevic J . Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles. Evolution. 2016; 71(2):274-288. DOI: 10.1111/evo.13109. View

13.

Rodriguez-Nuevo A, Torres-Sanchez A, Duran J, de Guirior C, Martinez-Zamora M, Boke E . Oocytes maintain ROS-free mitochondrial metabolism by suppressing complex I. Nature. 2022; 607(7920):756-761. PMC: 9329100. DOI: 10.1038/s41586-022-04979-5. View

14.

Feng J, Bussiere F, Hekimi S . Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev Cell. 2001; 1(5):633-44. DOI: 10.1016/s1534-5807(01)00071-5. View

15.

Miwa S, Jow H, Baty K, Johnson A, Czapiewski R, Saretzki G . Low abundance of the matrix arm of complex I in mitochondria predicts longevity in mice. Nat Commun. 2014; 5:3837. PMC: 4024759. DOI: 10.1038/ncomms4837. View

16.

Yang W, Hekimi S . Two modes of mitochondrial dysfunction lead independently to lifespan extension in Caenorhabditis elegans. Aging Cell. 2010; 9(3):433-47. DOI: 10.1111/j.1474-9726.2010.00571.x. View

17.

Rauthan M, Ranji P, Abukar R, Pilon M . A Mutation in Caenorhabditis elegans NDUF-7 Activates the Mitochondrial Stress Response and Prolongs Lifespan via ROS and CED-4. G3 (Bethesda). 2015; 5(8):1639-48. PMC: 4528320. DOI: 10.1534/g3.115.018598. View

18.

Nishimura A, Yoshikawa Y, Ichikawa K, Takemoto T, Tanahashi R, Takagi H . Longevity Regulation by Proline Oxidation in Yeast. Microorganisms. 2021; 9(8). PMC: 8400801. DOI: 10.3390/microorganisms9081650. View

19.

Kayser E, Sedensky M, Morgan P . The effects of complex I function and oxidative damage on lifespan and anesthetic sensitivity in Caenorhabditis elegans. Mech Ageing Dev. 2004; 125(6):455-64. DOI: 10.1016/j.mad.2004.04.002. View

20.

Barja G . Towards a unified mechanistic theory of aging. Exp Gerontol. 2019; 124:110627. DOI: 10.1016/j.exger.2019.05.016. View