DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Expanded Archaeal Genomes Shed New Light on the Evolution of Isoprenoid Biosynthesis

Journal Article · · Microorganisms

Isoprenoids and their derivatives, essential for all cellular life on Earth, are particularly crucial in archaeal membrane lipids, suggesting that their biosynthesis pathways have ancient origins and play pivotal roles in the evolution of early life. Despite all eukaryotes, archaea, and a few bacterial lineages being known to exclusively use the mevalonate (MVA) pathway to synthesize isoprenoids, the origin and evolutionary trajectory of the MVA pathway remain controversial. Here, we conducted a thorough comparison and phylogenetic analysis of key enzymes across the four types of MVA pathway, with the particular inclusion of metagenome assembled genomes (MAGs) from uncultivated archaea. Our findings support an archaeal origin of the MVA pathway, likely postdating the divergence of Bacteria and Archaea from the Last Universal Common Ancestor (LUCA), thus implying the LUCA’s enzymatic inability for isoprenoid biosynthesis. Notably, the Asgard archaea are implicated in playing central roles in the evolution of the MVA pathway, serving not only as putative ancestors of the eukaryote- and Thermoplasma-type routes, but also as crucial mediators in the gene transfer to eukaryotes, possibly during eukaryogenesis. Overall, this study advances our understanding of the origin and evolutionary history of the MVA pathway, providing unique insights into the lipid divide and the evolution of early life.

Research Organization:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Organization:
China Postdoctoral Science Foundation; National Natural Science Foundation of China; Shanghai Jiao Tong University 2030 Project; USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2471112
Journal Information:
Microorganisms, Journal Name: Microorganisms Journal Issue: 4 Vol. 12; ISSN 2076-2607
Publisher:
MDPICopyright Statement
Country of Publication:
United States
Language:
English

References (60)

Early Evolution of Membrane Lipids: How did the Lipid Divide Occur? journal January 2011
Diverse Asgard archaea including the novel phylum Gerdarchaeota participate in organic matter degradation journal March 2020
Expanding Asgard members in the domain of Archaea sheds new light on the origin of eukaryotes journal August 2021
Basic local alignment search tool journal October 1990
Structure and Mechanism of Homoserine Kinase journal December 2000
The phylogenetic distribution of the cell division system would not imply a cellular LUCA but a progenotic LUCA journal December 2021
Major New Microbial Groups Expand Diversity and Alter our Understanding of the Tree of Life journal March 2018
Crystal structure of mevalonate 3,5-bisphosphate decarboxylase reveals insight into the evolution of decarboxylases in the mevalonate metabolic pathways journal July 2022
Isoprenoid biosynthesis in Archaea – Biochemical and evolutionary implications journal January 2011
Construction and Optimization of Nonclassical Isoprenoid Biosynthetic Pathways in Yeast Peroxisomes for (+)-Valencene Production journal July 2023
Substrate Specificity and Engineering of Mevalonate 5-Phosphate Decarboxylase journal June 2019
Evidence of a Novel Mevalonate Pathway in Archaea journal June 2014
Complex archaea that bridge the gap between prokaryotes and eukaryotes journal May 2015
ModelFinder: fast model selection for accurate phylogenetic estimates journal May 2017
The early evolution of lipid membranes and the three domains of life journal June 2012
Comparative genomics, minimal gene-sets and the last universal common ancestor journal November 2003
The importance of biofilm formation for cultivation of a Micrarchaeon and its interactions with its Thermoplasmatales host journal April 2022
Phylogenomics provides robust support for a two-domains tree of life journal December 2019
Diversity, ecology and evolution of Archaea journal May 2020
Unique mobile elements and scalable gene flow at the prokaryote–eukaryote boundary revealed by circularized Asgard archaea genomes journal January 2022
Isolation of an archaeon at the prokaryote–eukaryote interface journal January 2020
Expanded diversity of Asgard archaea and their relationships with eukaryotes journal April 2021
Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes journal June 2023
An Adaptation To Life In Acid Through A Novel Mevalonate Pathway journal December 2016
Biosynthesis, evolution and ecology of microbial terpenoids journal January 2022
Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate journal October 1993
The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways journal August 2000
Modified mevalonate pathway of the archaeon Aeropyrum pernix proceeds via trans -anhydromevalonate 5-phosphate journal September 2018
Evolution of bacterial steroid biosynthesis and its impact on eukaryogenesis journal June 2021
Hybrid organic–inorganic structures trigger the formation of primitive cell-like compartments journal August 2023
Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes journal November 2000
( R )-Mevalonate 3-Phosphate Is an Intermediate of the Mevalonate Pathway in Thermoplasma acidophilum journal April 2014
GTDB-Tk v2: memory friendly classification with the genome taxonomy database journal October 2022
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
Biochemical evidence supporting the presence of the classical mevalonate pathway in the thermoacidophilic archaeon Sulfolobus solfataricus journal February 2013
IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era journal February 2020
Origins and Early Evolution of the Mevalonate Pathway of Isoprenoid Biosynthesis in the Three Domains of Life journal July 2010
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
On the Origin of Isoprenoid Biosynthesis journal June 2018
Tree Visualization By One Table (tvBOT): a web application for visualizing, modifying and annotating phylogenetic trees journal May 2023
Isoprenoids enhance the stability of fatty acid membranes at the emergence of life potentially leading to an early lipid divide journal October 2019
Biosynthesis of Isoprenoids via Mevalonate in Archaea: The Lost Pathway journal October 2000
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes journal May 2015
WebLogo: A Sequence Logo Generator journal May 2004
Origins and evolution of isoprenoid lipid biosynthesis in archaea journal March 2004
Discovery of integrons in Archaea: Platforms for cross-domain gene transfer journal November 2022
A rooted phylogeny resolves early bacterial evolution journal May 2021
Identification in Haloferax volcanii of Phosphomevalonate Decarboxylase and Isopentenyl Phosphate Kinase as Catalysts of the Terminal Enzyme Reactions in an Archaeal Alternate Mevalonate Pathway journal December 2013
Methanocaldococcus jannaschii Uses a Modified Mevalonate Pathway for Biosynthesis of Isopentenyl Diphosphate journal May 2006
Metagenomes from Coastal Marine Sediments Give Insights into the Ecological Role and Cellular Features of Loki - and Thorarchaeota journal October 2019
The 1-Deoxy-D-Xylulose-5-Phosphate Pathway of Isoprenoid Biosynthesis in Plants journal June 1999
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
The eukaryotic MEP-pathway genes are evolutionarily conserved and originated from Chlaymidia and cyanobacteria journal February 2021
Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits journal December 2022
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments journal March 2010
Evolutionary flexibility and rigidity in the bacterial methylerythritol phosphate (MEP) pathway journal November 2023
A Self-Assembled Aggregate Composed of a Fatty Acid Membrane and the Building Blocks of Biological Polymers Provides a First Step in the Emergence of Protocells journal August 2016
Deciphering Pathways for Carotenogenesis in Haloarchaea journal March 2020
Discovery of a metabolic alternative to the classical mevalonate pathway journal December 2013
An estimate of the deepest branches of the tree of life from ancient vertically evolving genes journal February 2022