Biology subjects

Martin, W. F.

Publications and source records attributed to Martin, W. F..

15 recordsLinked to original sources

bioRxiv2026

Metal-catalyzed phosphorylation by phosphite at the origin of bioenergetics

How did phosphate become the universal energetic currency of life? Traditional approaches to phosphorylation in early evolution studies entail oven drying, non-aqueous solvents, dangerously reactive forms of phosphorus, or other non-physiological conditions. With microbial physiology as a vade mecum, we have recently found that phosphite, HPO32-, which is enzymatically oxidized by many microbes and which naturally occurs in serpentinizing hydrothermal vents, will readily phosphorylate ribose, glucose, glycerol, serine, AMP, creatine and acetate to generate phosphoester, phosphoanhydride and acylphosphate bonds in hours to days at 25-100{degrees}C in pure alkaline water. These reactions are thermodynamically favourable because anoxic phosphite oxidation to phosphate and H2 is highly exergonic, but they do not proceed without catalysts. The most effective catalyst yet identified is a nanoparticular form of a shiny metal: zero-valent (native, or elemental) palladium (Pd0). Native palladium, like phosphite, also naturally occurs in serpentinizing hydrothermal vents, as do other native platinum group elements (PGE), including Pt, Rh, Ru and Ir. Here we test those PGE as catalysts of phosphite oxidation and phosphorylation. Though all metals tested readily oxidize phosphite, only Pd0 efficiently catalyzes phosphorylation, generating phosphorylated products at concentrations often equal to their physiological concentrations in growing Escherichia coli cells. Metaphosphate is a possible reaction intermediate. In phosphorylation reactions via phosphite oxidation (DG0'= -46 kJ{middle dot}mol-1), a portion of the energy released is conserved in phosphorylated products, as in biological energy conservation. A natural environment and energy-conserving thermodynamics implicate these facile aqueous phosphorylating reactions in the origin of bioenergetics.

evolutionary biology↗

bioRxiv2026

Prebiotic aqueous reactions catalyzed by native nickel without hydrogen

Compared to iron, nickel is comparatively rare as a transition metal in enzymes. But it is essential in several enzymes of carbon and energy metabolism in acetogens (bacteria) and methanogens (archaea), which use the acetyl-CoA pathway of H2-dependent CO2 fixation. Nickel containing enzymes of acetogens and methanogens include FeNi hydrogenase, carbon monoxide dehydrogenase, acetyl-CoA synthase and, in methanogens, methyl-CoM reductase in the last step of methane synthesis. Several lines of evidence implicate the acetyl-CoA pathway as the most ancient pathway of CO2 fixation, most notably recent findings that the overall reaction of the enzymatic pathway from H2 (E0' = -414 mV) and CO2 to pyruvate can be replaced by Ni0 alone in water as the lone catalyst. Here we studied the ability of Ni0 to serve as catalyst and reductant for nonenzymatic redox reactions that require only a mild reductant, as the midpoint potential of Ni0 oxidation to Ni2+ is E0' = -260 mV. We show that Ni0 in water can convert 2-oxo acids to 2-hydroxy acids and, in the presence of NH3, to amino acids at 25-100{degrees}C without addition of H2, and that it will function as catalyst and reductant for the fumarate reductase reaction. The findings expand the repertoire of ancient metabolic reactions that Ni0 can catalyze without proteins, cofactors, or sulfur, shedding light on the broad catalytic activity and substrate specificity of Ni0 at metabolic origin.

biochemistry↗

bioRxiv2025

Hydrothermal origin of metabolic phosphorylation

Phosphate is central to modern bioenergetics and to all theories for the origin of life. How phosphate entered metabolism is unknown, though microbial physiology and geochemical environments can provide important clues. Some bacteria obtain electrons and energy from phosphite (HPO32-), a reduced form of phosphate (HPO42-), that naturally occurs in serpentinizing (H2-producing) hydrothermal systems. Here we show that the insoluble, solid-state catalyst native palladium, which is naturally deposited in serpentinizing hydrothermal systems, catalyzes the oxidation of phosphite to phosphate and H2 in water at 25-100 {degrees}C in a highly exergonic reaction. Palladium awaruite (PdxNi3Fe), a common form of Pd0 in serpentinizing vents, also catalyzes phosphite-dependent phosphorylation. Phosphite oxidation over Pd0 generates a reactive but so far unidentified chemical intermediate, possibly metaphosphate, [PO3]-, that readily phosphorylates hydroxyl moieties in glycerol, ribose, glucose, serine and cytidine at 25-100 {degrees}C in 2-72 h. The same conditions also generate (i) phosphoanhydride bonds in pyrophosphate, polyphosphates and ADP, (ii) the phosphoramidate bond in phosphocreatine, (iii) and the acyl phosphate bond in acetyl phosphate, which is obtained overnight at 25 {degrees}C with 8% yield. The reactions proceed without sulfur, excluding thioester or metal sulfide intermediates. Phosphite-dependent phosphorylations under serpentinizing hydrothermal vent conditions are facile. They identify a natural, geochemical source of prebiotic phosphorylation and a novel source of metabolic energy at origins. The central role of phosphate in bioenergetics, metabolism, and nucleic acids could reflect metal-catalyzed, redox chemistry of phosphorus in the environment where metabolism (and life) arose.

microbiology↗

bioRxiv2024

The probability of a unique gene occurrence at the tips of a phylogenetic tree in the absence of horizontal gene transfer (the last-one-out)

Gene loss is an important process in gene and genome evolution. If a gene is present at the root of a rooted binary phylogenetic tree and can be lost in one descendant lineage, it can be lost in other descendant lineages as well, and potentially can be lost in all of them, leading to extinction of the gene on the tree. In that case, just before the gene goes extinct in the rooted phylogeny, there will be one lineage that still retains the gene for some period of time, representing a last-one-out distribution. If there are many (hundreds) of leaves in one clade of a phylogenetic tree, yet only one leaf possesses the gene, it will look like the result of a recent gene acquisition, even though the distribution at the tips was generated by loss. Here we derive the probability of observing last-one-out distributions under a Markovian loss model and a given gene loss rate {micro}. We find that the probability of observing such cases can be calculated mathematically, and can be surprisingly high, depending upon the tree and the rate of gene loss. Examples from real data show that gene loss can readily account for the observed frequency of last-one-out gene distribution patterns that might otherwise be attributed to lateral gene transfer.

evolutionary biology↗

bioRxiv2019

Gene duplications trace mitochondria to the onset of eukaryote complexity

The last eukaryote common ancestor (LECA) lived 1.6 billion years ago1,2. It possessed nuclei, sex, an endomembrane system, mitochondria, and all key traits that make eukaryotic cells more complex than their prokaryotic ancestors2-6. The closest known relatives of the host lineage that acquired the mitochondrion are, however, small obligately symbiotic archaea that lack any semblance of eukaryotic cell complexity7. Although the steep evolutionary grade separating prokaryotes from eukaryotes increasingly implicates mitochondrial symbiosis at eukaryote origin4,7, the timing and evolutionary significance of mitochondrial origin remains debated. Gradualist theories contend that eukaryotes arose from archaea by slow accumulation of eukaryotic traits8-10 with mitochondria arriving late11, while symbiotic theories have it that mitochondria initiated the onset of eukaryote complexity in a non-nucleated archaeal host7 by gene transfers from the organelle4,12-14. The evolutionary process leading to LECA should be recorded in its gene duplications. Among 163,545 duplications in 24,571 gene trees spanning 150 sequenced eukaryotic genomes we identified 713 gene duplication events that occurred in LECA. LECAs bacterially derived genes were duplicated more frequently than archaeal derived or eukaryote specific genes, reflecting the serial copying15,16 of genes from the mitochondrial endosymbiont to the archaeal hosts chromosomes prior to the onset of eukaryote genome complexity. Bacterial derived genes for mitochondrial functions, lipid synthesis, biosynthesis, as well as core carbon and energy metabolism in LECA were duplicated more often than archaeal derived genes and even more often than eukaryote-specific inventions for endomembrane, cytoskeletal or cell cycle functions. Gene duplications record the sequence of events at LECAs origin and indicate that recurrent gene transfer from a resident mitochondrial endosymbiont preceded the onset of eukaryotic cellular complexity.

evolutionary biology↗

bioRxiv2019

Bacterial genes outnumber archaeal genes in eukaryotic genomes

The origin of eukaryotes is one of evolutions most important transitions, yet it is still poorly understood. Evidence for how it occurred should be preserved in eukaryotic genomes. Based on phylogenetic trees from ribosomal RNA and ribosomal proteins, eukaryotes are typically depicted as branching together with or within archaea. This ribosomal affiliation is widely interpreted as evidence for an archaeal origin of eukaryotes. However, the extent to which the archaeal ancestry of genes for the cytosolic ribosomes of eukaryotic cells is representative for the rest of the eukaryotic genome is unknown. Here we have clustered 19,050,992 protein sequences from 5,443 bacteria and 212 archaea with 3,420,731 protein sequences from 150 eukaryotes spanning six eukaryotic supergroups to identify genes that link eukaryotes exclusively to bacteria and archaea respectively. By downsampling the bacterial sample we obtain estimates for the bacterial and archaeal proportions of genes among 150 eukaryotic genomes. Eukaryotic genomes possess a bacterial majority of genes. On average, eukaryotic genes are 56% bacterial in origin. The majority drops to 53% in eukaryotes that never possessed plastids, and increases to 61% in photosynthetic eukaryotic lineages, where the cyanobacterial ancestor of plastids contributed additional genes to the eukaryotic genome, reaching 67% in higher plants. Intracellular parasites, which undergo reductive evolution in adaptation to the nutrient rich environment of the cells that they infect, relinquish bacterial genes for metabolic processes. In the current sample, this process of adaptive gene loss is most pronounced in the human parasite Encephalitozoon intestinalis with 86% archaeal and 14% bacterial derived genes. The most bacterial eukaryote genome sampled is rice, with 67% bacterial and 33% archaeal genes. The functional dichotomy, initially described for yeast, of archaeal genes being involved in genetic information processing and bacterial genes being involved in metabolic processes is conserved across all eukaryotic supergroups.

evolutionary biology↗

bioRxiv2019

Anomalous phylogenetic behavior of ribosomal proteins in metagenome assembled genomes

Metagenomic studies have claimed the existence of novel lineages with unprecedented properties never before observed in prokaryotes. Such lineages include Asgard archaea1-3, which are purported to represent archaea with eukaryotic cell complexity, and the Candidate Phyla Radiation (CPR), a novel domain level taxon erected solely on the basis of metagenomic data4. However, it has escaped the attention of most biologists that these metagenomic sequences are not assembled into genomes by sequence overlap, as for cultured archaea and bacteria. Instead, short contigs are sorted into computer files by a process called binning in which they receive taxonomic assignment on the basis of sequence properties like GC content, dinucleotide frequencies, and stoichiometric co-occurrence across samples. Consequently, they are not genome sequences as we know them, reflecting the gene content of real organisms. Rather they are metagenome assembled genomes (MAGs). Debates that Asgard data are contaminated with individual eukaryotic sequences5-7 are overshadowed by the more pressing issue that no evidence exists to indicate that any sequences in binned Asgard MAGs actually stem from the same chromosome, as opposed to simply stemming from the same environment. Here we show that Asgard and CPR MAGs fail spectacularly to meet the most basic phylogenetic criterion8 fulfilled by genome sequences of all cultured prokaryotes investigated to date: the ribosomal proteins of Asgard and CPR MAGs do not share common evolutionary histories. Their phylogenetic behavior is anomalous to a degree never observed with genomes of real organisms. CPR and Asgard MAGs are binning artefacts, assembled from environments where up to 90% of the DNA is from dead cells9-12. Asgard and CPR MAGs are unnatural constructs, genome-like patchworks of genes that have been stitched together into computer files by binning.

evolutionary biology↗

bioRxiv2019

Mitochondria branch within Alphaproteobacteria

It is well accepted that mitochondria originated from an alphaproteobacterial-like ancestor. However, the phylogenetic relationship of the mitochondrial endosymbiont to extant alphaproteobacteria remains a subject of discussion. The focus of much debate is whether the affiliation between mitochondria and fast-evolving alphaproteobacterial lineages reflects true homology or artifacts. Approaches such as protein-recoding and site-exclusion have been claimed to mitigate compositional heterogeneity between taxa but this comes at the cost of information loss and the reliability of such methods is so far unjustified. Here we demonstrate that site-exclusion methods produce erratic phylogenetic estimates of mitochondrial origin. We applied alternative strategies to reduce phylogenetic noise by taxon replacement and selective exclusion while keeping site substitution information intact. Cross-validation based on a series of trees placed mitochondria robustly within Alphaproteobacteria.

evolutionary biology↗

bioRxiv2019

Autocatalytic chemical networks preceded proteins and RNA in evolution

Modern cells embody metabolic networks containing thousands of elements and form autocatalytic molecule sets that produce copies of themselves. How the first self-sustaining metabolic networks arose at life s origin is a major open question. Autocatalytic molecule sets smaller than metabolic networks were proposed as transitory intermediates at the origin of life, but evidence for their role in prebiotic evolution is lacking. Here we identify reflexively autocatalytic food-generated networks (RAFs)--self-sustaining networks that collectively catalyze all their reactions--embedded within microbial metabolism. RAFs in the metabolism of ancient anaerobic autotrophs that live from H2 and CO2 generate amino acids and bases, the monomeric components of protein and RNA, and acetyl-CoA, but amino acids and bases do not generate metabolic RAFs, indicating that small-molecule catalysis preceded polymers in biochemical evolution. RAFs uncover intermediate stages in the origin of metabolic networks, narrowing the gaps between early-Earth chemistry and life.

evolutionary biology↗

bioRxiv2019

A hydrogen dependent geochemical analogue of primordial carbon and energy metabolism

Hydrogen gas, H2, is generated in alkaline hydrothermal vents from reactions of iron containing minerals with water during a geological process called serpentinization. It has been a source of electrons and energy since there was liquid water on the early Earth, and it fuelled early anaerobic ecosystems in the Earths crust1-3. H2 is the electron donor for the most ancient route of biological CO2 fixation, the acetyl-CoA (or Wood-Ljungdahl) pathway, which unlike any other autotrophic pathway simultaneously supplies three key requirements for life: reduced carbon in the form of acetyl groups, electrons in the form of reduced ferredoxin, and ion gradients for energy conservation in the form of ATP4,5. The pathway is linear, not cyclic, it releases energy rather than requiring energy input, its enzymes are replete with primordial metal cofactors6,7, it traces to the last universal common ancestor8 and abiotic, geochemical organic syntheses resembling segments of the pathway occur in hydrothermal vents today9,10. Laboratory simulations of the acetyl-CoA pathways reactions include the nonenzymatic synthesis of thioesters from CO and methylsulfide11, the synthesis of acetate12 and pyruvate13 from CO2 using native iron or external electrochemical potentials14 as the electron source. However, a full abiotic analogue of the acetyl-CoA pathway from H2 and CO2 as it occurs in life has not been reported to date. Here we show that three hydrothermal minerals -- awaruite (Ni3Fe), magnetite (Fe3O4) and greigite (Fe3S4) -- catalyse the fixation of CO2 with H2 at 100 {degrees}C under alkaline aqueous conditions. The product spectrum includes formate (100 mM), acetate (100 M), pyruvate (10 M), methanol (100 M), and methane. With these simple catalysts, the overall exergonic reaction of the acetyl-CoA pathway is facile, shedding light on both the geochemical origin of microbial metabolism and on the nature of abiotic formate and methane synthesis in modern hydrothermal vents.

evolutionary biology↗

bioRxiv2019

Adaptation to life on land at 21% O2 via transition from ferredoxin- to NADH-dependent redox balance

Pyruvate:ferredoxin oxidoreductase (PFO) and iron only hydrogenase ([Fe]-HYD) are common enzymes among eukaryotic microbes that inhabit anaerobic niches. Their function is to maintain redox balance by donating electrons from food oxidation via ferredoxin (Fd) to protons, generating H2 as a waste product. Operating in series, they constitute a soluble electron transport chain of one-electron transfers between FeS clusters. They fulfill the same function -- redox balance -- served by two electron-transfers in the NADH- and O2-dependent respiratory chains of mitochondria. Although they possess O2-sensitive FeS clusters, PFO, Fd and [Fe]-HYD are also present among numerous algae that produce O2. The evolutionary persistence of these enzymes among eukaryotic aerobes is traditionally explained as enabling facultative anaerobic growth. Here we show that algae express enzymes of anaerobic energy metabolism at ambient O2 levels (21% v/v), Chlamydomonas reinhardtii expresses them with diurnal regulation. High O2 environments arose on Earth only some [~]450 million years ago. Gene presence absence and gene expression data indicate that during the transition to high O2 environments and terrestrialization, diverse algal lineages retained enzymes of Fd-dependent one-electron based redox balance, while the land plant and land animal lineages underwent irreversible specialization to redox balance involving the O2-insensitive two-electron carrier NADH.\n\nHighlights- Algae express enzymes of anaerobic metabolism in 21% [v/v] O2 atmosphere, independent of anaerobiosis\n- Retention of a plastid-encoded NADH dehydrogenase-like (NDH) was likely a prerequisite for the transition to life on land\n- Terrestrialization and adaption to high O2 is accompanied by a shift to redox balance at higher midpoint potentials\n- Eukaryotes adapted to high O2 life on land via specialization to two-electron based redox balance

evolutionary biology↗

bioRxiv2018

Nitrogenase inhibition limited oxygenation of the Proterozoic atmosphere

Cyanobacteria produced the atmospheric O2 that began accumulating 2.4 billion years ago1, leading to Earths Great Oxidation Event (GOE)2. For nearly 2 billion years following the GOE, O2 production was restricted and atmospheric oxygen remained low2-5. Oxygen rose again sharply with the advent of land plants roughly 450 million years ago, which increased atmospheric O2 through carbon burial4-5. Why did the O2 content of the atmosphere remain constant and low for more than a billion years despite the existence of O2-producing cyanobacteria? While geological limitations have been explored2-7, the limiting factor may have been biological, and enzymatic. Here we propose that O2 was kept low by oxygen inhibition of nitrogenase activity. Nitrogenase is the sole N2-fixing enzyme on Earth, and is inactive in air containing 2% or more O2 by volume8. No O2-resistant nitrogenase enzyme is known9-12. We further propose that nitrogenase inhibition by O2 kept atmospheric O2 low until upright terrestrial plants physically separated O2 production in aerial photosynthetic tissues from N2 fixation in soil, liberating nitrogenase from inhibition by atmospheric O2.

evolutionary biology↗

bioRxiv2018

Enlarged and highly repetitive plastome of Lagarostrobos and plastid phylogenomics of Podocarpaceae

Podocarpaceae is the largest family in cupressophytes (conifers II), but their plastid genomes (plastomes) are poorly studied, with plastome data currently existing for only four of the 19 Podocarpaceous genera. In this study, we assembled the plastomes from representatives of eight additional genera, including Afrocarpus, Dacrydium, Lagarostrobos, Lepidothamnus, Microstrobos, Phyllocladus, Prumnopitys, and Saxegothaea. We found that Lagarostrobos, a monotypic genus native to Tasmania, has the largest plastome among any cupressophytes studied to date (151,496 bp). Plastome enlargement in Lagarostrobos coincides with increased intergenic spacers, repeats, and duplicated genes. Among Podocarpaceae, Lagarostrobos has the most rearranged plastome, but its substitution rates are modest. Plastid phylogenomic analyses clarify the positions of previously conflicting Podocarpaceous genera. Tree topologies firmly support the division of Podocarpaceae into two sister clades: (1) the Prumnopityoid clade and (2) the clade containing Podocarpoid, Dacrydioid, Microstrobos, and Saxegothaea. The Phyllocladus is nested within the Podocarpaceae, thus familial status of the monotypic Phyllocladaceae is not supported.

evolutionary biology↗

bioRxiv2018

Lipids are the preferred substrate of the protist Naegleria gruberi, relative of a human brain pathogen

Naegleria gruberi is a free-living non-pathogenic amoeboflagellate and relative of Naegleria fowleri, a deadly pathogen causing primary amoebic meningoencephalitis (PAM). A genomic analysis of N. gruberi exists, but physiological evidence for its core energy metabolism or in vivo growth substrates is lacking. Here we show that N. gruberi trophozoites need oxygen for normal functioning and growth and that they furthermore shun both glucose and amino acids as growth substrates. Trophozoite growth depends mainly upon lipid oxidation via a mitochondrial branched respiratory chain, both ends of which require oxygen as final electron acceptor. Growing N. gruberi trophozoites thus have a strictly aerobic energy metabolism with a marked substrate preference for the oxidation of fatty acids. Analyses of N. fowleri genome data and comparison with those of N. gruberi indicate that N. fowleri has the same type of metabolism. Specialization to oxygen-dependent lipid breakdown represents a hitherto unprecedented metabolic strategy in protists.

biochemistry↗

bioRxiv2018

Count does not recover major events of gene flux in real biological data

In prokaryotes, known mechanisms of lateral gene transfer (transformation, transduction, conjugation and gene transfer agents) generate new combinations of genes among chromosomes during evolution. In eukaryotes, whose host lineage is descended from archaea, lateral gene transfer from organelles to the nucleus occurs at endosymbiotic events. Recent genome analyses studying gene distributions have uncovered evidence for sporadic, discontinuous events of gene transfer from bacteria to archaea during evolution. Other studies have used traditional birth-and-death phylogenetic models to investigate prokaryote genome evolution to claim that gene transfer to archaea was continuous during evolution, rather than involving occasional periodic mass gene influx events. Here we test the ability of Count, a birth-and-death based program, to recover known events of mass acquisition and differential loss using plastid genomes and eukaryotic protein families that were acquired from plastids. Count showed a strong bias towards reconstructed histories having gene acquisitions distributed uniformly across the tree. Sometimes as many as nine different acquisitions by plastid DNA were inferred for the same protein family. That is, Count recovered gradual and continuous lateral gene transfer among lineages, even when massive gains followed by gradual differential loss is the true evolutionary process that generated the gene distribution data.

evolutionary biology↗