Evolution of Physiology: The link between Earth and Life

The history of life is a subject that attracts the interest from both researchers and the society in general - it is in the human nature to wonder about our own history. Our only sources of information about microbial evolution reside in genomic data and geological records. Major advances in sequencing techniques are overwhelming databases with rich and novel insights into microbial taxonomic diversity, in particular about new uncultured lineages. Through metagenomics we now know that they are there but we still do not understand what they are doing.The key to that understanding is not genomics, it is physiology.Our main impediment to understand environmental microbial life is our lack of insights into the physiology of newly discovered lineages, how they harness and conserve energy.While phylogenetic trees based on universal genes can be generated for thousands of lineages at a time, they do not represent the genome as a whole and, most importantly, due to lateral gene transfer, branching patterns in the tree of life have never correlated well with key physiological traits.The goal of this proposal, whose focus is physiology, is to better understand how microbes harness energy from available environmental sources, how they learned to use new ones, and how this process unfolded during microbial evolution.This will involve i) large-scale comparative phylogenetic analysis of genes involved in and genomically associated with physiology combined with ii) experimental data, using as evolutionary constraints geochemical records of available environmental energy sources.With a top-down approach this work will successively eliminate among extant biological traits ones that cannot be ancient, constraining the physiological space of older microbial solutions.This proposal will lead to testable predictions regarding the order of events in evolutionary bioenergetic transitions, the focus on biological energy harnessing will narrow the gap between geochemistry and microbiology.

Duration: 01.02.2019-31.01.2025

Funding agency: ERC Starting Grant

Project leader: Dr. Filipa Sousa

Participants: Filipa Sousa, Angus Hilts, Caroline Ivesic, Inga Iziumova, Val Karavaeva, Leandro Nascimento Lemos, Ulf Naumann, Sinje Neukirchen, Rafael Isaac Ponce Toledo, Joost van Ham

For more information, please see here.

    Peer-reviewed publications related to or funded through this project

    • Rodrigues-Oliveira T, Wollweber F, Ponce-Toledo RI, Xu J, Rittmann SKR, Klingl A, Pilhofer M, Schleper C. (2023) Actin cytoskeleton and complex cell architecture in an Asgard archaeon. Nature. 2023 Jan;613(7943):332-339. doi: 10.1038/s41586-022-05550-y. Epub 2022 Dec 21. PMID: 36544020; PMCID: PMC9834061.
    • Zamarreño Beas J, Videira MAM, Karavaeva V, Lourenço FM, Almeida MR, Sousa F, Saraiva LM. (2023) In Campylobacter jejuni, a new type of chaperone receives heme from ferrochelatase. Front Genet. 2023 Jun 21;14:1199357. doi: 10.3389/fgene.2023.1199357. PMID: 37415606; PMCID: PMC10320005.
    • Neukirchen S, Pereira IAC, Sousa FL. (2023) Stepwise pathway for early evolutionary assembly of dissimilatory sulfite and sulfate reduction. ISME J. 2023 Oct;17(10):1680-1692. doi: 10.1038/s41396-023-01477-y. Epub 2023 Jul 19. PMID: 37468676; PMCID: PMC10504309.
    • Karavaeva V, Sousa FL. (2023) Modular structure of complex II: An evolutionary perspective. Biochim Biophys Acta Bioenerg. 2023 Jan 1;1864(1):148916. doi: 10.1016/j.bbabio.2022.148916. Epub 2022 Sep 6. PMID: 36084748.
    • Videira MAM, Lobo SAL, Sousa FL, Saraiva LM. (2020) Identification of the sirohaem biosynthesis pathway in Staphylococcus aureus. FEBS J. 2020 Apr;287(8):1537-1553. doi: 10.1111/febs.15091. Epub 2019 Oct 27. PMID: 31605669.
    • Preiner M, Asche S, Becker S, Betts HC, Boniface A, Camprubi E, Chandru K, Erastova V, Garg SG, Khawaja N, Kostyrka G, Machné R, Moggioli G, Muchowska KB, Neukirchen S, Peter B, Pichlhöfer E, Radványi Á, Rossetto D, Salditt A, Schmelling NM, Sousa FL, Tria FDK, Vörös D, Xavier JC. (2020) The Future of Origin of Life Research: Bridging Decades-Old Divisions. Life (Basel). 2020 Feb 26;10(3):20. doi: 10.3390/life10030020. PMID: 32110893; PMCID: PMC7151616.
    • Chernyh NA, Neukirchen S, Frolov EN, Sousa FL, Miroshnichenko ML, Merkel AY, Pimenov NV, Sorokin DY, Ciordia S, Mena MC, Ferrer M, Golyshin PN, Lebedinsky AV, Cardoso Pereira IA, Bonch-Osmolovskaya EA. (2020) Dissimilatory sulfate reduction in the archaeon 'Candidatus Vulcanisaeta moutnovskia' sheds light on the evolution of sulfur metabolism. Nat Microbiol. 2020 Nov;5(11):1428-1438. doi: 10.1038/s41564-020-0776-z. Epub 2020 Aug 17. PMID: 32807893.