An early origin of iron–sulfur cluster biosynthesis machineries before Earth oxygenation

Nature Ecology & Evolution, Год журнала: 2022, Номер 6(10), С. 1564 - 1572

Опубликована: Сен. 15, 2022

Язык: Английский

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The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers

Environmental Microbiome, Год журнала: 2021, Номер 16(1)

Опубликована: Дек. 1, 2021

The highly diverse Cand. Patescibacteria are predicted to have minimal biosynthetic and metabolic pathways, which hinders understanding of how their populations differentiate in response environmental drivers or host organisms. Their mechanisms employed cope with oxidative stress largely unknown. Here, we utilized genome-resolved metagenomics investigate the adaptive genome repertoire oxic anoxic groundwaters, infer putative ranges.Within six groundwater wells, was most dominant (up 79%) super-phylum across 32 metagenomes sequenced from DNA retained on 0.2 0.1 µm filters after sequential filtration. Of reconstructed 1275 metagenome-assembled genomes (MAGs), 291 high-quality MAGs were classified as Patescibacteria. Paceibacteria Microgenomates enriched exclusively fractions, whereas candidate division ABY1 Gracilibacteria fractions. On average, smaller filter fractions had 22% genomes, 13.4% lower replication measures, higher proportion rod-shape determining proteins, genomic features suggesting type IV pili mediated cell-cell attachments. Near-surface wells harbored rates than downstream characterized by longer water residence time. Except prevalence superoxide dismutase genes groundwaters (83%), no major phylogenetic differences observed. abundant MAG encoded a nitrate transporter, nitrite reductase, F-type ATPase, an alternative energy conservation mechanism. consistently co-occurred one another members phyla Nanoarchaeota, Bacteroidota, Nitrospirota, Omnitrophota. Among fractions,, only 8% showed significant one-to-one correlation, mostly Motility transport related certain similar other (Omnitrophota, Proteobacteria Nanoarchaeota).Other stress, found little evidence for niche adaptation groundwaters. Given that could detect specific preference few MAGs, speculate majority is able attach multiple hosts just long enough loot exchange supplies.

Язык: Английский

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Engineering functional thermostable proteins using ancestral sequence reconstruction

Journal of Biological Chemistry, Год журнала: 2022, Номер 298(10), С. 102435 - 102435

Опубликована: Авг. 27, 2022

Natural proteins are often only slightly more stable in the native state than denatured state, and an increase environmental temperature can easily shift balance toward unfolding. Therefore, engineering of to improve protein stability is area intensive research. Thermostable required withstand industrial process conditions, for increased shelf-life therapeutics, developing robust 'biobricks' synthetic biology applications, research purposes (e.g., structure determination). In addition, thermostability buffers destabilizing effects mutations introduced other properties. Rational design approaches require structural information, but even with advanced computational methods, it challenging predict or parameterize all relevant factors sufficient precision anticipate results a given mutation. Directed evolution alternative when structures unavailable requires extensive screening mutant libraries. Recently, however, bioinspired based on phylogenetic analyses have shown great promise. Leveraging rapid expansion sequence data bioinformatic tools, ancestral reconstruction generate highly folds novel applications chemistry, medicine, biology. This review provides overview important successful inference thermostable by what reveal about determinants proteins. Native complex three-dimensional arrangements functional groups, which evolved carry out discrete biological functions that almost always depend maintenance specific spatial relationships. However, typically represent metastable between conformational flexibility be disturbed such as heat, organic solvents, chaotropic agents, pH (1Pace C.N. Conformational globular proteins.Trends Biochem. Sci. 1990; 15: 14-17Abstract Full Text PDF PubMed Scopus (387) Google Scholar). Both enthalpic entropic determine how linear polymer amino acid residues reproducibly into structure, including intramolecular interactions different elements degree solvation polar hydrophobic regions (2Baker D. What has de novo taught us folding biophysics?.Protein 2019; 28: 678-683Crossref (85) Any change affect these therefore alter ability polypeptide chain fold structure. Nature explored small proportion available space, so there much scope engineer useful most must domains (3Bommarius A.S. Paye M.F. Stabilizing biocatalysts.Chem. Soc. Rev. 2013; 42: 6534-6565Crossref (320) Scholar, 4Burton S.G. Cowan D.A. Woodley J.M. The search ideal biocatalyst.Nat. Biotech. 2002; 20: 37-45Crossref (0) Scholar) (an exception being intrinsically disordered proteins), so, understanding underpin essential effective design. Studies scaffolds better able accept potentially confer activities properties (5Tokuriki N. Tawfik D.S. Stability evolvability.Curr. Opin. Struct. Biol. 2009; 19: 596-604Crossref (494) 6Socha R.D. Tokuriki Modulating - directed strategies improved function.FEBS J. 280: 5582-5595Crossref (67) Indeed robustness key factor behind power law describing extent been exploited evolution: inherently observed commonly (7Magner A. Szpankowski W. Kihara On origin superfamilies superfolds.Sci. Rep. 2015; 5: 8166Crossref (14) Enzymes particular case where produced versatile catalysts lower activation energy chemical reactions. Just nature, industry, enzymes potential efficiency sustainability many processes. Increasing operational reactions improves yield reduces waste enhancing reaction rates, improving reagent solubility reducing microbial contamination; limited under their normal physiological conditions rapidly at elevated temperatures. Since biocatalyst (i.e., enzyme cell containing it) expensive part biocatalytic process, commercially competitive against chemocatalysis, used need long lifetimes While from thermophilic organisms one option, rarely possible find thermophile catalytic profile interest. 'mesophilic' usually needs extended, efforts over last ∼40 years put thermostable. Industrial biocatalysis not motivation stabilizing however. also found wide application basic research, example, PCR due use polymerases, originally sourced thermophiles, enable iterative replication amplification DNA templates. development numerous therapeutics provided added impetus types thermostability. longer shelf life wider range therapeutic contexts less More recently, emergence expanded independently biobricks devices. Yet another homologs needed mechanistic studies, since they expressed purified, stand up biophysical characterization. analysis thermophiles valuable information stabilize folds, interest become clear success stabilization dependent context. Good rational available, alternative, 'blind' approach characterization large libraries mutants. Fortuitously, source inspiration nature emerged recent years, namely resurrection enzymes, alongside consensus approaches, leverages huge genome sequencing projects. will briefly summarize traditional thermostability, then explore (ASR) strategy elucidation free difference folded unfolded states ∼5 15 kcal/mol few protein. determining appropriate changes make, without unwanted function, ongoing challenge. Figure 1 compares terms required, typical effort space sampled. methods involved designing core packing, salt bridges, disulfide bonds. Alternatively constraining flexible shortening loops, replacing glycine, introducing proline useful. Critically, rely having involve some hypothesis basis putative effect. vary context presented individual affected landscape epistatic interactions. facilitated tools (reviewed (6Socha 8Dombkowski A.A. Sultana K.Z. Craig D.B. Protein engineering.FEBS Lett. 2014; 588: 206-212Crossref (162) 9Pongsupasa V. Anuwan P. Maenpuen S. Wongnate T. Rational-design thermostability.in: Magnani F. C M. F Enzyme Engineering: Methods Protocols. Humana Press, New York, NY2022: 159-178Crossref (2) 10Modarres H.P. Mofrad M.R. Sanati-Nezhad engineering.RSC Adv. 2016; 6: 115252-115270Crossref 11Ó'Fágáin C. Engineering stability.in: Walls Loughran S.T. Chromatography: NY2011: 103-136Crossref (25) 12Weinstein Khersonsky O. Fleishman S.J. Practically protein-design combining atomistic calculations.Curr. 2020; 63: 58-64Crossref (21) 13Eijsink V.G.H. Bjork Gaseidnes Sirevag R. Synstad B. van den Burg et al.Rational stability.J. Biotechnol. 2004; 113: 105-120Crossref (375) 14Eijsink Borchert T.V. stability.Biomol. Eng. 2005; 22: 21-30Crossref (339) 15Steipe Consensus-based stability: intrabodies enzymes.Protein 388: 176-186Crossref (57) 16Razvi Scholtz Lessons proteins.Protein 2006; 1569-1578Crossref (267) 17Wijma H.J. Floor R.J. Janssen Structure- sequence-analysis inspired enhanced thermostability.Curr. 23: 588-594Crossref (145) 18Sun Z.T. Liu Q. Qu G. Feng Y. Reetz M.T. Utility B-factors science: interpreting rigidity, flexibility, internal motion thermostability.Chem. 119: 1626-1665Crossref (206) Scholar), achieved notable successes (19Aalbers F.S. Fürst M.J.L.J. Rovida Trajkovic Gómez Castellanos J.R. Bartsch al.Approaching boiling point alcohol dehydrogenase through computationally-guided engineering.eLife. 9: e54639Crossref (20) was ∼94 °C). Many machine learning databases training data. cases, quality determines accuracy biased mutation (10Modarres Current difficulty modeling critical alterations 20Huang Chu S.K.S. Frizzo H.N. Connolly M.P. Caster R.W. Siegel J.B. Evaluating prediction using generated dataset.ACS Omega. 6487-6493Crossref (22) Expansion standardization databases, plus high throughput afford comprehensive obtained comparable deep mutational scanning combinatorial (21Nisthal Wang C.Y. Ary M.L. Mayo S.L. insights revealed domain-wide mutagenesis.Proc. Natl. Acad. U. 116: 16367-16377Crossref (59) may facilitate predictions augmenting Artificial intelligence AlphaFold (22Jumper Evans Pritzel Green Figurnov Ronneberger al.Highly accurate AlphaFold.Nature. 2021; 596: 583-589Crossref (5177) should make likely lead step change. Importantly, predicts inputs them, PROSS (23Goldenzweig Goldsmith Hill S.E. Gertman Laurino Ashani al.Automated structure- sequence-based bacterial expression stability.Mol. Cell. 337-346Abstract (223) 1990s 'brute force' technique independent any prior concerning mechanism stabilization. It mimics natural selection rounds genetic diversification (such random mutagenesis recombination related sequences) combined phenotypic thermal absence base hypotheses, stability, targeted saturation mutagenesis. employing entirely detect mutants (Fig. 1). to, assess activity stringent fashion, detailed melting temperatures (Tms) half population remains intact active (T50 values) resource intensive. focus smaller, fertile areas sought. identifying target B-factor (24Reetz Carballeira J.D. Vogel Iterative B increasing thermostability.Angew. Chem. Int. Ed. 45: 7745-7751Crossref Scholar)) structure-guided (25Romero P.A. Arnold F.H. Random field model reveals recombinational landscape.PLoS Comput. 2012; 8e1002713Crossref (8) 26Romero Krause Navigating fitness Gaussian processes.Proc. 110: E193-E201Crossref (151) deleterious neutral beneficial (27Guo H.H. Choe Loeb L.A. tolerance change.Proc. 101: 9205-9210Crossref (226) places limit number (typically two, maximum) per sequence, iteration. relatively around starting mutagenesis, likelihood accrue naturally occurring sequences sample larger volume space. Such enriched since, always, residue position naturally, is, 'vetted' least parents (not eliminated purifying selection). homologous diverged evolutionary branches acquired relationships fold, incompatible fragments recombined, leading loss introduction steric clashes electrostatic repulsion. Computational applied strategies, just particular, structure-based average integrity created recombinatorial evolution. Chief amongst SCHEMA, uses representative estimate optimal positions minimize disruption (28Voigt C.A. Martinez Z.G. building blocks preserved recombination.Nat. 553-558PubMed 29Otey C.R. Silberg J.J. Voigt Endelman Bandara Functional conservation chimeric cytochromes P450: calibrating approach.Chem. 11: 309-318Abstract (87) extension this approach, processes, Bayesian trained 242 measurements cytochrome P450 chimeras SCHEMA allowed identification showed further 5.3 °C T50 (26Romero identified 'augmented' differ points dozens hundreds positions, meaning would readily conventional methods. respect, analogous optimization enabled Rosetta (re)design. 'algorithm', leveraging evolutionarily proven Over ∼25 implicit pathways emerged, ASR. Assuming function confers growth advantage organism, tend select destabilize Thus, unlikely frankly destabilizing, unless of, greater than, marginally dominate long-term (30Steipe Schiller Plückthun Steinbacher Sequence statistics reliably domain.J. Mol. 1994; 240: 188-192Crossref (273) 31Bershtein Goldin K. Intense drifts evolvable proteins.J. 2008; 379: 1029-1044Crossref (194) studies taken 'consensus' 32Amin A.D. Ramer Aehle Meijer Metin al.Construction stabilized mutagenesis.Protein Des. Sel. 17: 787-793Crossref (120) 33Lehmann Loch Middendorf Studer Lassen S.F. Pasamontes L. al.The concept proteins: proof concept.Protein 403-411Crossref 34Lehmann Wyss proteins.Biochim. Biophys. Acta. 2000; 1543: 408-415Crossref 35Kohl Binz H.K. Forrer Stumpp Grütter M.G. Designed stable: crystal ankyrin repeat protein.Proc. 2003; 100: 1700-1705Crossref (234) 36Sullivan B.J. Durani Magliery T.J. Triosephosphate Isomerase design: dramatic differences physical variants.J. 2011; 413: 195-208Crossref (45) 37Rath Davidson A.R. hyperstable Abp1p SH3 domain alignment analysis.Protein 2457-2469Crossref (50) 38Di Nardo Larson S.M. relationship conservation, thermodynamic core.J. 333: 641-655Crossref (56) Scholar); One set sequences. heavily imbalances amount certain relative others. Consequently, hard dissociate stochastic historical true position. ASR frequently yielded ancestor extant counterparts, providing support primordial were thermophilic. earliest example 3-isopropylmalate (IPMDH) universal common (39Miyazaki Nakaya Suzuki Tamakoshi Oshima Yamagishi Ancestral extreme thermophile: experimental evidence supporting hypothesis.J. 2001; 129: 777-782Crossref Seven IPMDH thermophile, Sulfolobus strain 7, form, idea thermophile. Multiple complete elongation Tu (EF Tu) Precambrian (>∼500 million ago; Ma) bacteria (40Gaucher E.A. Thomson Burgan Benner S.A. Inferring palaeoenvironment ancient resurrected proteins.Nature. 425: 285-288Crossref (197) inferred phylogeny consisting forms mesophilic, thermophilic, hyperthermophilic bacteria. EF node representing mesophilic substrate-binding ∼55 compared ∼37 basal lineages substrate binding (∼65 °C) thermophiles. Analysis seven intermediate ancestors trend progressively going back time 0.5 3.5 billion ago (Ga); Tm values youngest ∼44 48 ∼65 74 oldest (41Gaucher Ganesh O.K. Govindarajan Palaeotemperature 451: 704-707Crossref (264) foundational work followed similar sets various ages assessed means assessing existence (42Akanuma Nakajima Yokobori Kimura Nemoto Mase al.Experimental thermophilicity life.Proc. 11067-11072Crossref (119) 43Garcia A.K. Schopf J.W. S.-i. Akanuma Reconstructed suggest cooling Earth's photic zone Archean.Proc. 2017; 114: 4619Crossref 44Iwabata H. Watanabe Ohkuri Thermostability Caldococcus noboribetus isocitrate dehydrogenase.FEMS Microbiol. 243: 393-398Crossref thermophily (45Hobbs J.K. Shepherd Saul D.J. Demetras N.J. Haaning Monk al.On thermophily: Bacillus.Mol. Evol. 29: 825-835Crossref (62) 46Hart K.M. Harms M.J. Schmidt B.H. Elya Thornton Marqusee Thermodynamic system drift evolution.PLoS. 12e1001994Crossref (51) 47Nguyen Wilson Hoemberger Stiller Agafonov R.V. Kutter al.Evolutionary drivers thermoadaptation catalysis.Science. 355: 289-293Crossref (109) exploring (48Perez-Jimenez Inglés-Prieto Zhao Z. Sanchez-Romero I. Alegre-Cebollada Kosuri al.Single-molecule paleoenzymology probes chemistry enzymes.Nat. 18: 592-596Crossref (152) 49Risso V.A. Gavira J.A. Mejia-Carmona D.F. Gaucher Sanchez-Ruiz Hyperstability promiscuity laboratory resurrections β-lactamases.J. Am. 135: 2899-2902Crossref (170) These covered broad families, taxa (bacteria eukarya; plants, animals, fungi), (from hundred thousand four old). prevailing observation mesostable today forms. Enhancements directly ranged degrees 40 2; Table re

Язык: Английский

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A divide-and-conquer phylogenomic approach based on character supermatrices resolves early steps in the evolution of the Archaea

BMC Ecology and Evolution, Год журнала: 2022, Номер 22(1)

Опубликована: Янв. 5, 2022

The recent rise in cultivation-independent genome sequencing has provided key material to explore uncharted branches of the Tree Life. This been particularly spectacular concerning Archaea, projecting them at center stage as prominently relevant understand early stages evolution and emergence fundamental metabolisms well origin eukaryotes. Yet, resolving deep divergences remains a challenging task due well-known tree-reconstruction artefacts biases extracting robust ancient phylogenetic signal, notably when analyzing data sets including three Domains Among various strategies aimed mitigating these problems, divide-and-conquer approaches remain poorly explored, have primarily based on reconciliation among single gene trees which however notoriously lack signal.We analyzed sub-sets full supermatrices covering whole Life with specific taxonomic sampling robustly resolve different parts archaeal phylogeny light their current diversity. Our results strongly support existence two main clades, Cluster I II, we name Ouranosarchaea Gaiarchaea, clarify placement important novel lineages within clades. However, monophyly branching fast evolving nanosized DPANN members unclear worth further study.We inferred resolved rooted Archaea that includes all recently described phyla high rank. represents valuable reference study evolutionary events associated steps diversification domain. Beyond specifics phylogeny, our demonstrate power relationships, should be applied progressively entire

Язык: Английский

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An ancient divide in outer membrane tethering systems in bacteria suggests a mechanism for the diderm-to-monoderm transition

Nature Microbiology, Год журнала: 2022, Номер 7(3), С. 411 - 422

Опубликована: Март 4, 2022

Язык: Английский

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ATP synthase evolution on a cross-braced dated tree of life

Nature Communications, Год журнала: 2023, Номер 14(1)

Опубликована: Ноя. 17, 2023

Abstract The timing of early cellular evolution, from the divergence Archaea and Bacteria to origin eukaryotes, is poorly constrained. ATP synthase complex thought have originated prior Last Universal Common Ancestor (LUCA) analyses genes, together with ribosomes, played a key role in inferring rooting tree life. We reconstruct evolutionary history synthases using an expanded taxon sampling set develop phylogenetic cross-bracing approach, constraining equivalent speciation nodes be contemporaneous, based on imprint endosymbioses ancient gene duplications. This approach results highly resolved, dated species establishes absolute timeline for evolution. Our show that into F- A/V-type lineages was very event evolution dating back more than 4 Ga, potentially predating diversification Bacteria. cross-braced, life also provides insight recent transitions including eukaryogenesis, showing eukaryotic nuclear mitochondrial diverged their closest archaeal (2.67-2.19 Ga) bacterial (2.58-2.12 relatives at approximately same time, slightly longer stem-lineage.

Язык: Английский

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Gene gain facilitated endosymbiotic evolution of Chlamydiae

Nature Microbiology, Год журнала: 2023, Номер 8(1), С. 40 - 54

Опубликована: Янв. 5, 2023

Abstract Chlamydiae is a bacterial phylum composed of obligate animal and protist endosymbionts. However, other members the Planctomycetes–Verrucomicrobia–Chlamydiae superphylum are primarily free living. How transitioned to an endosymbiotic lifestyle still largely unresolved. Here we reconstructed species relationships modelled genome evolution. Gene content reconstruction from 11,996 gene families suggests motile facultatively anaerobic last common ancestor that had already gained characteristic endosymbiont genes. Counter expectations for streamlining in strict endosymbionts, detected substantial gain within Chlamydiae. We found divergence energy metabolism aerobiosis observed extant lineages emerged later during chlamydial In particular, metabolic aerobic genes more metabolically versatile protist-infecting chlamydiae were gained, such as respiratory chain complexes. Our results show complexity can increase evolution, adding additional perspective understanding symbiont evolutionary trajectories across tree life.

Язык: Английский

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Ancient origin and constrained evolution of the division and cell wall gene cluster in Bacteria

Nature Microbiology, Год журнала: 2022, Номер 7(12), С. 2114 - 2127

Опубликована: Ноя. 21, 2022

Язык: Английский

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The Evolution and Evolvability of Photosystem II

Annual Review of Plant Biology, Год журнала: 2023, Номер 74(1), С. 225 - 257

Опубликована: Март 8, 2023

Photosystem II is the water-oxidizing and O2-evolving enzyme of photosynthesis. How when this remarkable arose are fundamental questions in history life that have remained difficult to answer. Here, recent advances our understanding origin evolution photosystem reviewed discussed detail. The indicates water oxidation originated early life, long before diversification cyanobacteria other major groups prokaryotes, challenging transforming current paradigms on We show has virtually unchanged for billions years, yet nonstop duplication process D1 subunit II, which controls photochemistry catalysis, enabled become adaptable variable environmental conditions even innovate enzymatic functions beyond oxidation. suggest evolvability can be harnessed develop novel light-powered enzymes with capacity carry out complex multistep oxidative transformations sustainable biocatalysis.

Язык: Английский

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Large-scale phylogenomics of aquatic bacteria reveal molecular mechanisms for adaptation to salinity

Science Advances, Год журнала: 2023, Номер 9(21)

Опубликована: Май 26, 2023

The crossing of environmental barriers poses major adaptive challenges. Rareness freshwater-marine transitions separates the bacterial communities, but how these are related to brackish counterparts remains elusive, as do molecular adaptations facilitating cross-biome transitions. We conducted large-scale phylogenomic analysis freshwater, brackish, and marine quality-filtered metagenome-assembled genomes (11,248). Average nucleotide identity analyses showed that species rarely existed in multiple biomes. In contrast, distinct basins cohosted numerous species, their intraspecific population structures displayed clear signs geographic separation. further identified most recent transitions, which were rare, ancient, commonly directed toward biome. Transitions accompanied by systematic changes amino acid composition isoelectric point distributions inferred proteomes, evolved over millions years, well convergent gains or losses specific gene functions. Therefore, challenges entailing proteome reorganization content constrains resulting species-level separation between aquatic

Язык: Английский

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