Periodic Reporting for period 4 - EvolPhysiol (Evolution of Physiology: The link between Earth and Life)
Reporting period: 2023-08-01 to 2025-01-31
As humans, we wonder about our history. We wonder how, at a certain place and a certain time, life arose within a lifeless planet. From that time on, life has evolved to reach today’s levels of biodiversity, in where microbes have learned a multitude of different ways to get nutrients from their surroundings and survive. However, the exact ways microbes nowadays explore the environment in terms of how they conserve their energy and obtain nutrients from the surroundings are highly diverse, and still not fully understood. From an evolutionary point, it is clear that all of this diversity did not arise at once. Thus, stepwise transitions, from simpler to more complex energy harnessing solutions, must have existed. 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. Moreover, backbone tree based approaches assume that genes within genomes tend to share the same evolutionary history. It is becoming increasingly clear that the evolution of microbial traits, the evolution of bioenergetics processes, is decoupled from the evolution of ribosomal lineages, mainly due to Lateral Gene Transfer (LGT).
The goal of this project was to better understand how microbes harness energy from their environment, how they learned to use new ones, and how this process unfolded during microbial evolution. This involved large-scale comparative phylogenetic analysis of genes involved in, and genomically associated with, energy-harnessing systems combined with experimental data, using as evolutionary constraints geochemical records of available environmental energy sources.
The goal of this project was to better understand how microbes harness energy from their environment, how they learned to use new ones, and how this process unfolded during microbial evolution. This involved large-scale comparative phylogenetic analysis of genes involved in, and genomically associated with, energy-harnessing systems combined with experimental data, using as evolutionary constraints geochemical records of available environmental energy sources.
From the beginning of the project to its conclusion, progress was made in mapping bioenergetic systems in prokaryotes, elucidating the modular nature of energy-converting protein complexes, tracing the evolution of cofactor biosynthesis, experimentally characterising novel complexes, and developing evolutionary models for transitions between bioenergetic systems. Below is an overview of the work performed and the main results achieved, along with their exploitation and dissemination.
The project made substantial advances in understanding the diversity and ecological roles of Asgard archaea, which are central to bridging prokaryotic and eukaryotic evolution. The publication "Diversity and environmental distribution of Asgard archaea in shallow saline sediments" (Frontiers in Microbiology) revealed their involvement in carbon and sulfur cycling, providing insights into their metabolic diversity. Additionally, "Actin cytoskeleton and complex cell architecture in an Asgard archaeon" (Nature) uncovered structural features such as actin-like cytoskeletal proteins, positioning Asgard archaea as evolutionary intermediates between prokaryotes and eukaryotes. These findings have advanced our understanding of archaeal contributions to eukaryogenesis and ecological adaptations.
The study "Modular structure of complex II: An evolutionary perspective" (BBA-Bioenergetics) explored the modular organization of succinate:quinone oxidoreductase (Complex II), demonstrating how modularity drives functional evolution in bioenergetic systems. This work highlighted how modular architectures enhance adaptability and robustness in energy-converting protein complexes, providing a framework for understanding their evolutionary diversification. This modularity was also observed in the case of the evolution of sulfate reduction within the archaea, where modules from methanogenic organisms and not other sulfate reducers were recruited and adapted by convergent evolution to create an archaeal-Qmo complex.
The publication "Evidence for corrin biosynthesis in the last universal common ancestor" (The FEBS Journal) traced corrinoid biosynthesis to LUCA (Last Universal Common Ancestor), linking cofactor evolution to ancient metabolic pathways critical for early bioenergetics. Papers currently in preparation explore the emergence and diversification of heme biosynthesis pathways essential for oxygen-dependent energy metabolism, as well as molybdenum cofactor (MoCo) biosynthesis systems that play central roles in modern bioenergetic processes. These results provide foundational insights into how cofactors essential for life originated and evolved.
Several enzymatic proteins were characterised including hybrid hydrogenases from archaea (Cell), expanding knowledge about enzymatic diversity and activity critical for energy metabolism. Another publication (Protein Science), investigated modular assembly principles within sulfur-metabolizing complexes, contributing to a deeper understanding of enzymatic mechanisms driving sulfur-based bioenergetics. In addition, a new chaperon involved in heme metabolism (Front. Genetics) and a novel protein involved in NO detoxification were also characterized (Sci. Reports).
The study "Stepwise pathway for early evolutionary assembly of dissimilatory sulfite and sulfate reduction" (The ISME Journal) proposed a model linking ancestral sulfur-based pathways to modern ones. Similarly, "Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism" (Nature Microbiology) identified evolutionary intermediates bridging ancestral and modern sulfur metabolism pathways.
The overall findings of the project regarding the modularity of protein blocks and reuse of cofactors were synthesized into a broader framework connecting Earth’s geochemical history to life’s bioenergetic evolution in the accepted paper "Bioenergetics Evolution: The link between Earth’s and Life’s history" (Phil. Trans. R. Soc. B- accepted).
Exploitation and Dissemination: The results from this project were disseminated through publications in high-impact journals such as Nature, Cell, Nature Microbiology, The ISME Journal, and others. These publications have reached diverse audiences across microbiology, biochemistry, structural biology, and evolutionary biology communities. The findings have also been presented at international conferences, fostering collaborations with peers.Beyond academic dissemination, computational tools developed during the project (e.g. bioinformatic pipelines for predicting bioenergetic gene clusters) are available to other researchers to support further studies.
The project made substantial advances in understanding the diversity and ecological roles of Asgard archaea, which are central to bridging prokaryotic and eukaryotic evolution. The publication "Diversity and environmental distribution of Asgard archaea in shallow saline sediments" (Frontiers in Microbiology) revealed their involvement in carbon and sulfur cycling, providing insights into their metabolic diversity. Additionally, "Actin cytoskeleton and complex cell architecture in an Asgard archaeon" (Nature) uncovered structural features such as actin-like cytoskeletal proteins, positioning Asgard archaea as evolutionary intermediates between prokaryotes and eukaryotes. These findings have advanced our understanding of archaeal contributions to eukaryogenesis and ecological adaptations.
The study "Modular structure of complex II: An evolutionary perspective" (BBA-Bioenergetics) explored the modular organization of succinate:quinone oxidoreductase (Complex II), demonstrating how modularity drives functional evolution in bioenergetic systems. This work highlighted how modular architectures enhance adaptability and robustness in energy-converting protein complexes, providing a framework for understanding their evolutionary diversification. This modularity was also observed in the case of the evolution of sulfate reduction within the archaea, where modules from methanogenic organisms and not other sulfate reducers were recruited and adapted by convergent evolution to create an archaeal-Qmo complex.
The publication "Evidence for corrin biosynthesis in the last universal common ancestor" (The FEBS Journal) traced corrinoid biosynthesis to LUCA (Last Universal Common Ancestor), linking cofactor evolution to ancient metabolic pathways critical for early bioenergetics. Papers currently in preparation explore the emergence and diversification of heme biosynthesis pathways essential for oxygen-dependent energy metabolism, as well as molybdenum cofactor (MoCo) biosynthesis systems that play central roles in modern bioenergetic processes. These results provide foundational insights into how cofactors essential for life originated and evolved.
Several enzymatic proteins were characterised including hybrid hydrogenases from archaea (Cell), expanding knowledge about enzymatic diversity and activity critical for energy metabolism. Another publication (Protein Science), investigated modular assembly principles within sulfur-metabolizing complexes, contributing to a deeper understanding of enzymatic mechanisms driving sulfur-based bioenergetics. In addition, a new chaperon involved in heme metabolism (Front. Genetics) and a novel protein involved in NO detoxification were also characterized (Sci. Reports).
The study "Stepwise pathway for early evolutionary assembly of dissimilatory sulfite and sulfate reduction" (The ISME Journal) proposed a model linking ancestral sulfur-based pathways to modern ones. Similarly, "Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism" (Nature Microbiology) identified evolutionary intermediates bridging ancestral and modern sulfur metabolism pathways.
The overall findings of the project regarding the modularity of protein blocks and reuse of cofactors were synthesized into a broader framework connecting Earth’s geochemical history to life’s bioenergetic evolution in the accepted paper "Bioenergetics Evolution: The link between Earth’s and Life’s history" (Phil. Trans. R. Soc. B- accepted).
Exploitation and Dissemination: The results from this project were disseminated through publications in high-impact journals such as Nature, Cell, Nature Microbiology, The ISME Journal, and others. These publications have reached diverse audiences across microbiology, biochemistry, structural biology, and evolutionary biology communities. The findings have also been presented at international conferences, fostering collaborations with peers.Beyond academic dissemination, computational tools developed during the project (e.g. bioinformatic pipelines for predicting bioenergetic gene clusters) are available to other researchers to support further studies.
The results lead us to made progress in the field and change some of the given concepts in the field such as for instance, the evolution of sulfate reduction within the archaea, or the proposed existence of complex II in Luca. It also allowed us to access how automatic functional annotation tools deal with the diversity of metagenomic data available and pinpoint gaps in knowledge.
The results from this project strengthened ties between geochemistry and microbiology, and hence stimulate the dialogue across disciplines to further our understanding of Life – a subject that attracts the interest from both researchers and the society in general.
The results from this project strengthened ties between geochemistry and microbiology, and hence stimulate the dialogue across disciplines to further our understanding of Life – a subject that attracts the interest from both researchers and the society in general.