Biology subjects

McGlynn, S. E.

Publications and source records attributed to McGlynn, S. E..

9 recordsLinked to original sources

bioRxiv2023

Scaling of Protein Function Across the Tree of Life

Scaling laws are a powerful way to compare genomes because they put all organisms onto a single curve and reveal non-trivial generalities as genomes change in size. The abundance of functional categories in a given genome scales with genome size, suggesting that universal constraints shape category abundance. Here we look across the tree of life to understand how genome evolution may be related to functional scaling. We revisit previous observations of functional genome scaling with an expanded taxonomy by analyzing 3726 bacterial, 220 archaeal, and 79 unicellular eukaryotic genomes. We find that for some functional classes, scaling is best described by multiple exponents, revealing previously unobserved shifts in scaling as genomes grow or contract. Furthermore, scaling varies between phyletic groups and is less universal than previously thought, with scaling shifts varying uniquely between domains and scaling exponents varying uniquely between phyla. We also find that individual phyla frequently span scaling exponents of functional classes, revealing that individual clades can move across scaling exponents. Across the tree of life, variability in functional scaling is not accounted for by genome phylogeny, suggesting that physiological and/or cell plan outweighs phylogeny.

evolutionary biology↗

bioRxiv2022

Continuity between ancient geochemistry and modern metabolism enabled by non-autocatalytic purine biosynthesis

A major unresolved question in the origin and evolution of life is whether a continuous path from geochemical precursors to the majority of molecules in the biosphere can be reconstructed from modern day biochemistry. Here we simulated the emergence of ancient metabolic networks and identified a feasible path from simple geochemically plausible precursors (e.g., phosphate, sulfide, ammonia, simple carboxylic acids, and metals) using only known biochemical reactions and models of primitive coenzymes. We find that purine synthesis constitutes a bottleneck for metabolic expansion, and that non-autocatalytic phosphoryl coupling agents are necessary to enable expansion from geochemistry to modern metabolic networks. Our model predicts punctuated phases of metabolic evolution characterized by the emergence of small molecule coenzymes (e.g., ATP, NAD+, FAD). Early phases in the resulting expansion are associated with enzymes that are metal dependent and structurally symmetric, supporting models of early biochemical evolution. This expansion trajectory produces distinct hypotheses regarding the timing and mode of metabolic pathway evolution, including a late appearance of methane metabolisms and oxygenic photosynthesis consistent with the geochemical record. The concordance between biological and geological analysis suggests that this trajectory provides a plausible evolutionary history for the vast majority of core biochemistry.

systems biology↗

bioRxiv2021

Evidence for the Emergence of β-Trefoils by 'Peptide Budding' from an IgG-like β-Sandwich

As sequence and structure comparison algorithms gain sensitivity, the intrinsic interconnectedness of the protein universe has become increasingly apparent. Despite this general trend, {beta}-trefoils have emerged as an uncommon counterexample: They are an isolated protein lineage for which few, if any, sequence or structure associations to other lineages have been identified. If {beta}-trefoils are, in fact, remote islands in sequence-structure space, it implies that the oligomerizing peptide that founded the {beta}-trefoil lineage itself arose de novo. To better understand {beta}-trefoil evolution, and to probe the limits of fragment sharing across the protein universe, we identified both {beta}-trefoil bridging themes (evolutionarily-related sequence segments) and {beta}-trefoil-like motifs (structure motifs with a hallmark feature of the {beta}-trefoil architecture) in multiple, ostensibly unrelated, protein lineages. The success of the present approach stems, in part, from considering {beta}-trefoil sequence segments or structure motifs rather than the {beta}-trefoil architecture as a whole, as has been done previously. The newly uncovered inter-lineage connections presented here suggest a novel hypothesis about the origins of the {beta}-trefoil fold itself - namely, that it is a derived fold formed by budding from an Immunoglobulin-like {beta}-sandwich protein. These results demonstrate how the emergence of a folded domain from a peptide need not be a signature of antiquity and underpin an emerging truth: few protein lineages escape natures sewing table.

bioinformatics↗

bioRxiv2020

Complex history of aerobic respiration and phototrophy in the Chloroflexota class Anaerolineae revealed by high-quality draft genome of Ca. Roseilinea mizusawaensis AA3_104

The candidate genus Roseilinea is a novel lineage in the Chloroflexota (formerly Chloroflexi or green nonsulfur bacteria) phylum known so far only from very incomplete metagenome-assembled genomes and preliminary enrichments. Roseilinea is notable for appearing capable of anoxygenic photoheterotrophy despite being only distantly related to well-known phototrophic Chloroflexota in the Chloroflexia class such as Chloroflexus and Roseiflexus. Here, we present a high quality metagenome-assembled genome of a member of Roseilinea, greatly improving our understanding of the metabolic capacity and taxonomic assignment of this genus. These data allow us to confidently describe the genetic basis for photoheterotrophy in these organisms as well as propose a candidate family for these organisms, Ca. Roseilineaceae, within the Anaerolineae class of Chloroflexota.

microbiology↗

bioRxiv2020

Changes in ATP sulfurylase activityin response to altered cyanobacteria growth conditions.

Here we investigated variations in cell growth and ATP sulfurylase activity when two cyanobacterial strains - Synechocystis sp. PCC6803 and Synechococcus sp. WH7803 - were grown comparatively between conventional media and media with low ammonium, low sulfate and a controlled high CO2/low O2 atmosphere, which might resemble some Precambrian environments. In both organisms, a transition and adaptation to the reconstructed environmental media resulted in a decrease in ATPS specific activity. This decrease in activity appears to be decoupled from growth rate, suggesting the enzyme is not rate-limiting in S assimilation and raising questions about the role of ATPS redox regulation in cell physiology and thorughout history.

physiology↗

bioRxiv2020

The Thermosynechococcus genus: wide environmental distribution, but a highly conserved genomic core

Cyanobacteria thrive in very diverse environments. However, questions remain about possible growth limitations in ancient environmental conditions. As a single genus, the Thermosynechococcus are cosmopolitan and live in chemically diverse habitats. To understand the genetic basis for this, we compared the protein coding component of Thermosynechococcus genomes. Supplementing the known genetic diversity of Thermosynechococcus, we report draft metagenome-assembled genomes of two Thermosynechococcus recovered from ferrous carbonate hot springs in Japan. We find that as a genus, Thermosynechococcus is genomically conserved, having a small pan-genome with few accessory genes per individual strain and only 14 putative orthologous protein groups appearing in all Thermosynechococcus but not in any other cyanobacteria in our analysis. Furthermore, by comparing orthologous protein groups, including an analysis of genes encoding proteins with an iron related function (uptake, storage or utilization), no clear differences in genetic content, or adaptive mechanisms could be detected between genus members, despite the range of environments they inhabit. Overall, our results highlight a seemingly innate ability for Thermosynechococcus to inhabit diverse habitats without having undergone substantial genomic adaptation to accommodate this. The finding of Thermosynechococcus in both hot and high iron environments without adaptation recognizable from the perspective of the proteome has implications for understanding the basis of thermophily within this clade, and also for understanding the possible genetic basis for high iron tolerance in cyanobacteria on early Earth. The conserved core genome may be indicative of an allopatric lifestyle - or reduced genetic complexity of hot spring habitats relative to other environments.

genomics↗

bioRxiv2020

CO2 reduction driven by a pH gradient

All life on Earth is built of organic molecules, so the primordial sources of reduced carbon are a major open question in studies of the origin of life. A variant of the alkaline-vent theory suggests that organics could have been produced by the reduction of CO2 via H2 oxidation, facilitated by geologically sustained pH gradients. The process would be an abiotic analog--and proposed evolutionary predecessor--of the modern Wood-Ljungdahl acetyl-Co-A pathway of extant archaea and bacteria. The first energetic bottleneck of the pathway involves the endergonic reduction of CO2 with H2 to formate, which has proven elusive in low-temperature abiotic settings. Here we show the reduction of CO2 with H2 at moderate pressures (1.5 bar), driven by microfluidic pH gradients across inorganic Fe(Ni)S precipitates. Isotopic labelling with 13C confirmed production of formate. Separately, deuterium (2H) labelling indicated that electron transfer to CO2 did not occur via direct hydrogenation with H2. Instead, freshly deposited Fe(Ni)S precipitates appear to facilitate electron transfer in an electrochemical-cell mechanism with two distinct half-reactions. Decreasing the pH gradient significantly, or removing either H2 or the precipitate, yielded no detectable product. Our work demonstrates the feasibility of spatially separated, yet electrically coupled geochemical reactions as drivers of otherwise endergonic processes. Beyond corroborating the ability of early-Earth alkaline hydrothermal systems to couple carbon reduction to hydrogen oxidation through geologically plausible and biologically relevant mechanisms, these results may also be of significance for industrial and environmental applications, where other redox reactions could be facilitated using similarly mild approaches.

biochemistry↗

bioRxiv2019

Phototrophic Methane Oxidation in a Member of the Chloroflexi Phylum

Biological methane cycling plays an important role in Earths climate and the global carbon cycle, with biological methane oxidation (methanotrophy) modulating methane release from numerous environments including soils, sediments, and water columns. Methanotrophy is typically coupled to aerobic respiration or anaerobically via the reduction of sulfate, nitrate, or metal oxides, and while the possibility of coupling methane oxidation to phototrophy (photomethanotrophy) has been proposed, no organism has ever been described that is capable of this metabolism. Here we described a new bacterial genome from a member of the Chloroflexi phylum--termed here Candidatus Chlorolinea photomethanotrophicum--with cooccurring methanotrophy and phototrophy pathways, suggesting a novel link between these two metabolisms. Recovered as a metagenome-assembled genome from microbial mats in an iron-rich hot spring in Japan, Ca. C. photomethanotrophicum forms a new lineage within the Chloroflexi phylum and expands the known metabolic diversity of this already diverse clade. Ca. C. photomethanotrophicum appears to be metabolically versatile, capable of phototrophy (via a Type 2 reaction center), aerobic respiration, nitrite reduction, oxidation of methane and carbon monoxide, and potentially carbon fixation via a novel pathway composed of hybridized components of the serine cycle and the 3-hydroxypropionate bicycle. The biochemical network of this organism is constructed from components from multiple organisms and pathways, further demonstrating the modular nature of metabolic machinery and the ecological and evolutionary importance of horizontal gene transfer in the establishment of novel pathways. SignificanceMethane is a major greenhouse gas, and the production and consumption of methane is largely driven by the metabolism of microorganisms. Although it has been hypothesized for decades that some bacteria may be capable of growth by eating methane and conserving energy from sunlight (photomethanotrophy), this metabolism has never been discovered in nature. Here, we describe the first genetic evidence for a bacterium capable of photomethanotrophy, adding a new pathway to the known diversity of how microbes can make a living. This discovery also adds a new link to the global carbon cycle, and may provide new opportunities for designing biotechnological tools for processing methane.

microbiology↗

bioRxiv2018

Thermophilic Lithotrophy and Phototrophy in an Intertidal, Iron-rich, Geothermal Spring

Hydrothermal systems, including terrestrial hot springs, contain diverse geochemical conditions that vary over short spatial scales due to progressive interaction between the reducing hydrothermal fluids, the oxygenated atmosphere, and in some cases seawater. At Jinata Onsen, on Shikinejima Island, Japan, an intertidal, anoxic, iron-rich hot spring mixes with the oxygenated atmosphere and seawater over short spatial scales, creating a diversity of chemical potentials and redox pairs over a distance ~10 m. We characterized the geochemical conditions along the outflow of Jinata Onsen as well as the microbial communities present in biofilms, mats, and mineral crusts along its traverse via 16S rDNA amplicon and genome-resolved shotgun metagenomic sequencing. The microbial community changed significantly downstream as temperatures and dissolved iron concentrations decreased and dissolved oxygen increased. Near the spring source, biomass is limited relative to downstream, and primary productivity may be fueled by oxidation of ferrous iron and molecular hydrogen by members of the Zetaproteobacteria and Aquificae. Downstream, the microbial community is dominated by oxygenic Cyanobacteria. Cyanobacteria are abundant and active even at ferrous iron concentrations of ~150 M, which challenges the idea that iron toxicity limited cyanobacterial expansion in Precambrian oceans. Several novel lineages of Bacteria are also present at Jinata Onsen, including previously uncharacterized members of the Chloroflexi and Caldithrichaeota phyla, positioning Jinata Onsen as a valuable site for future characterization of these clades. ImportanceHigh temperatures and reducing conditions allow hot springs to support microbial communities that are very different from those found elsewhere on the surface of the Earth today; in some ways, these environments and the communities they support can be similar to environments that existed on the early Earth and that may exist on other planets. Here, we describe a novel hot spring system where hot, iron-rich but oxygen-poor water flows into the ocean, supporting a range of unique microbial communities. Metagenomic sequencing recovered many novel microbial lineages, including deep-branching and uniquely thermotolerant members of known groups. Comparison of the biological communities in the upstream part of the hot spring, potentially supported by biological iron and hydrogen oxidizing metabolisms, to downstream microbial mats, supported by oxygenic photosynthesis, provides insight into the potential productivity of life during Proterozoic time and on other planets where oxygenic photosynthesis is not possible.

microbiology↗