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    Global warming leads to larger bats with a faster life history pace in the long-lived Bechstein’s bat (Myotis bechsteinii)

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    Country Compendium of the Global Register of Introduced and Invasive Species

    GRIIS and the Country CompendiumThe Global Register of Introduced and Invasive Species (GRIIS) arose following recognition of the need for a product of this nature in discussions on implementation of the Convention on Biological Diversity (CBD). In 2011, a joint work programme to strengthen information services on invasive alien species as a contribution towards Aichi Biodiversity Target 9 was developed19. The Global Invasive Alien Species Information Partnership (GIASI Partnership) was then established to assist Parties to the CBD, and others, to implement Article 8(h) and Target 9 of the Aichi Biodiversity Targets. The Conference of Parties (COP-11) welcomed the development of the GIASI Partnership and requested the Executive Secretary to facilitate its implementation (paragraph 22 of decision XI/28). In 2013, the development of GRIIS was identified as a key priority to be led by the IUCN ISSG and Partners built on a prototype initiated almost a decade earlier (Item 4, Report of the Global Invasive Alien Species Information Partnership, Steering Committee, 1st meeting Montreal, 15 October 2013)20.GRIIS is a database of discrete checklists of alien species that are present in specified geographic units (including not only countries, but also as yet unpublished checklists of islands, offshore territories, and protected areas) (Fig. 1). The GRIIS Country Compendium is a collation and key product that derives and is updatable from the working GRIIS Research Database that underpins this and other GRIIS products (Fig. 1). Individual checklists are published to GBIF through an installation of the Integrated Publishing Toolkit21 (IPT) and hosted by the GBIF Secretariat. Exceptions include the Belgium (hosted by the Research Institute for Nature and Forest) and U.S.A checklists (hosted by the United States Geological Survey). Data are published as Darwin Core (dwc namespace) Archive files and the terms and structure follow that standard exchange format22.The GRIIS Country Compendium is an aggregation of 196 GRIIS country checklists of which 82% have been verified by Country Editors (see13), along with revised and additional fields that enable global level analysis and country and taxon comparisons (Tables 2, 3). Checklists for the 196 countries were combined into a single file (Table 3). A field was added to indicate which country the checklist belonged to, and the ISO 3116-1 Alpha-2 and Alpha-3 country codes are included to facilitate dataset integration (see ‘Usage notes’) (Table 2). A field was also added to indicate the verification status of each checklist (Table 2). The ID field was renamed (originally ‘taxonID’ and now ‘recordID’), as the data now represent a country-level occurrence dataset containing multiple records per species, rather than checklist-type data that contains one record per species. In total, the data now include 18 fields as described in Table 2, encompassing taxonomic, location, habitat, occurrence, introduced and invasive alien status (see also Table 1). This publication represents a versioned, citable snapshot of the Compendium (Fig. 1) that is ready for analysis and integration with other data sources (e.g. workflow23 and ‘Example applications of the Compendium’ outlined further below).Table 2 Fields and field terms in the GRIIS Country Compendium.Full size tableTable 3 Countries in the GRIIS Country Compendium and their review status.Full size tablePopulation of data fields in GRIISThe methods by which GRIIS is populated were described in 201813 and are summarised in brief here. A systematic decision-making process is used for each geographic unit by species record to designate non-native origin and evidence of impact (see Fig. 2 in Pagad et al.13). Comprehensive searches are undertaken for each country. Records are included from the earliest documented to the most recent accessed record prior to the date of the latest published checklist version. Information sources include peer-reviewed scientific publications, national checklists and databases, reports containing results of surveys of alien and invasive alien species, general reports (including unpublished government reports), and datasets held by researchers and practitioners13. A log of the changes to each checklist is available on the GBIF IPT24, with the changes to the Belgium checklist available at the INBO IPT25. The most up to date version of each checklist is thus available via GBIF.org, as is a list of all GRIIS checklists at GBIF.org24.Fig. 2Summary of data in the GRIIS Country Compendium. Number of invasive alien species by major taxonomic group (a) and habitat (b). Number of records per major taxonomic groups (c) and habitat (d). The number of species and records associated with invasion impact (i.e. isInvasive) are shown in black. Note different y-axis scales in each case.Full size imageIntroduced species of all taxonomic groups are considered for inclusion in GRIIS. Habitats include terrestrial, freshwater, brackish, marine and also host (i.e. for species that are not free-living) (Table 2, Pagad et al.13). The habitat information in GRIIS (Table 2) is sourced from taxon and region-specific databases such as WoRMS (World Register of Marine Species), FishBase, Pacific Island Ecosystems at Risk, and the USDA Plants Database. Typically, GRIIS records are at the species level, but in some cases, other ranks are more appropriate including infraspecies (including forms, varieties and subspecies). A separate field is provided for hybrids (Table 2). Where species are present and both native to parts of a country and alien in other parts of the country, their introduction status (dwc:establishmentMeans) is included as Native|Alien (Tables 1, 2)26. If there is limited knowledge about the Origin of the species, its introduction status (dwc:establishmentMeans) is included as Cryptogenic|Uncertain (Tables 1, 2).Two types of evidence are considered to assign a species by country record as invasive (Table 1, see also Pagad et al.13): (i) when any authoritative source (e.g. from the primary literature or unpublished reports from country/species experts), describe an environmental impact, and/or (ii) when any source determines the species to be widespread, spreading rapidly or present in high abundance (based on the assumption that cover, abundance, high rates of population growth or spread are positively correlated with impact)27,28. Each record is assigned either invasive or null in the isInvasive field to reflect the presence of evidence of impact, or absence of evidence of impact (note, not ‘evidence of absence of impact’), for that species by country record (Table 2). In the future this information may be supplemented with impact scores29,30,31. Finally, a draft checklist is sent to Country Editors for validation and revision (see Technical Validation).Taxonomic harmonization and normalizationThe use of different synonyms across countries to refer to the same taxonomic concept is frequent32. The species in each Country Checklist were thus harmonised against the GBIF Backbone Taxonomy33. The names in each checklist were matched using a custom script that integrates with the GBIF API34, and the accepted name, taxon rank, status and higher taxonomy (Table 2) were obtained at this stage. Spelling and other errors in assigning species authorship were corrected where appropriate.To validate the taxonomic harmonisation, every name variant present in the GRIIS Country Compendium was checked against the GBIF Backbone Taxonomy using the API33. A unique list of names (i.e. acceptedName Usage) was thus produced and the source name retained as ‘scientificName’ (that can differ across countries) (Table 2). Over 95% of names across all kingdoms matched exactly at 98% or greater confidence (Table 4). All names that were below 98% confidence or had a match type other than ‘Exact’ were checked and modified if appropriate to do so. Of the non-matches (n = 253, those with a match type of ‘None’), most were formulaic hybrid names of plants and animals (~62%), which are not officially supported by GBIF35. The remaining non-matches were names of mostly plants (17%), but also animals (8%), viruses (8%) and chromists (3%).Table 4 Taxonomic matching results (percentages) by Kingdom using the GBIF Backbone Taxonomy33.Full size tableData summaryThere are currently ~23 700 species represented by 101 000 taxon-country combination records, across 196 countries in the GRIIS Country Compendium. All raw numbers are provided to the nearest order of magnitude to reflect the taxonomic uncertainty and dynamic nature of GRIIS (see ‘Known data gaps and uncertainties’). The vast majority of records are at the species level (97.6%), with the remaining present as subspecies (1.7%), varieties (0.6%), genera (0.1%) and forms ( More

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    Shell thickness of Nucella lapillus in the North Sea increased over the last 130 years despite ocean acidification

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    Expanding the phylogenetic distribution of cytochrome b-containing methanogenic archaea sheds light on the evolution of methanogenesis

    Discovery of a novel archaeal lineage in wetland sedimentsTo examine archaeal community composition and function in a mangrove ecosystem, we analyzed metagenomic data from 13 sediment samples taken from mangrove wetlands in Techeng Island of Zhanjiang and Dongzhai Harbour of Haikou, China (Supplementary Fig. 1). De novo assembly of these sequencing data (60–120 Gbp for each sample) and genome binning resulted in 242 archaeal MAGs ( >70% complete; 85.4% AAI) detected in two metagenomes in IMG database generated from sediments of Lake Towuti, Indonesia (Supplementary Fig. 1 and Supplementary Table 2). Two additional related MAGs (TDP8 and TDP10, Table 1) encoding the complete Mcr complex were subsequently recovered from these metagenomes. For these MAGs (with exception of HK01M), the mcrABG operon and other genes related to methane metabolism were located on long contigs (≥11,476 bp) whose sequence composition features were consistent with their corresponding genomes (Supplementary Fig. 3), supporting the accurate assignment of these contigs to each MAG. The estimated genome size range for the seven MAGs recovered was 1.06–2.55 Mbp with total number of coding sequences ranging from 1151 to 3291. We examined vertical distribution of these MAGs in sediment cores of two sampling sites and found that their relative abundance increased gradually as depth increased from 15 to 100 cm (Supplementary text; Supplementary Fig. 4). Subsequent searches of public sequencing databases using the 16S rRNA and mcrA gene sequences annotated in these MAGs identified related species in freshwater lake sediments, hot springs, mangrove wetlands, rice paddy soils, hydrothermal vents, and deep-sea sediments distributed in different regions of the world (Supplementary text; Supplementary Table 3 and Supplementary Fig. 5).Phylogenomic analysis using 122 concatenated archaeal-specific marker proteins revealed that the seven MAGs and “Ca. M. tengchongensis” formed a distinct lineage that is sister to the order Nitrososphaerales (Fig. 1a and Supplementary Fig. 2b). Phylogenetic analyses of the 16S and 23S rRNA genes recovered from these MAGs supported the novelty of this lineage (Supplementary Table 4 and Supplementary Fig. 2a), with pairwise nucleotide comparisons of 16S rRNA genes revealing an identity of 79.1–87.3% to publicly available Nitrososphaeria genomes (Supplementary Table 5). The seven MAGs belonging to the novel lineage had an AAI of 44.0–52.3% to all other genomes of the Nitrososphaeria (Supplementary Table 6), further supporting their classification as a separate order [21, 22]. Collectively, these phylogenetic analyses indicate that these MAGs represent four different genera of the recently described family “Ca. Methylarchaceae” within a novel order—designated here as “Ca. Methylarchaeales” (Fig. 1a and Supplementary Fig. 2 and Supplementary Tables 5 and 6). H03B1, HK01M, HK01B, and HK02M1 represents one genus (69.7–80% AAI to other MAGs), HK02M2 represents the second (68.9–80% AAI to other MAGs), TDP8 and TDP10 represent the third (70.2–82.5% AAI), and “Ca. M. tengchongensis” represents the fourth (68.9–82.5% AAI); the former three genera are named here “Ca. Methanoinsularis”, “Ca. Methanoporticola”, and “Ca. Methanotowutia”, respectively.The “Ca. Methylarchaeales” are potentially methyl-reducing methanogens with b-type cytochromesAnnotation of the eight “Ca. Methylarchaeales” MAGs confirmed genes involved in archaeal methane metabolism (Supplementary Table 7 and Fig. 2), including those encoding the Mcr complex (mcrABG and auxiliary genes mcrCD), and the ATP-binding protein AtwA (component A2) required for Mcr activation [23]. The “Ca. Methylarchaeales” harbor genes for methane production from methanol and methylamines (mtaA, mtbA, mttB, mtbB, and mtmB) (Supplementary Table 7 and Fig. 2), suggesting that the “Ca. Methylarchaeales” have potential to perform methyl-reducing methanogenesis, as previously suggested for “Ca. M. tengchongensis” [7], and members of the orders Methanomassiliicoccales [15], “Ca. Methanofastidiosales” [19] and “Ca. Methanomethylicales” [4]. All of the “Ca. Methylarchaeales” MAGs encoded a tetrahydromethanopterin (H4MPT) S-methyltransferase subunit H (MtrH), and either a MtrX or MtrA, that are homologous to those of Methanosarcina barkeri (Supplementary Table 7). Phylogenetic analysis revealed that the “Ca. Methylarchaeales” MtrH subunits are more closely related to a MtrH (BP07_RS03240) of Methermicoccus shengliensis than to the MtrH subunits of Methanosarcina (Supplementary Fig. 6). It is likely that the “Ca. Methylarchaeales” MtrH may be involved in methyl transfer directly to H4MPT, as previously shown in M. shengliensis for utilization of methoxylated aromatic compounds [24]. The absence of a complete gene operon for Mtr complex suggests that the “Ca. Methylarchaeales” cannot use the CO2 reduction or aceticlastic pathway for methanogenesis.Fig. 2: Proposed metabolic pathways in the “Ca. Methylarchaeales”.Genes found in H03B1/HK01M/HK01B/ HK02M1 (blue-green dots), HK02M2 (pink dots), TDP8/TDP10 (green dots), and JZ-2-bin_220 (brown dots) or missing from all bins (gray) are indicated. Genes associated with these pathways and their full name are provided in Supplementary Table 7. MP Methanophenazine, Fd ferredoxin, b-cyt b-type cytochrome.Full size imageIn contrast to the “Ca. Methanomethylicales”, all genes for the Wood-Ljundahl pathway (WLP) and acetyl-CoA decarbonylase/synthase: CO dehydrogenases (ACDS/CODH) are also present in all the genomes (Supplementary Table 7 and Fig. 2). However, we did not identify the energy-converting hydrogenase complex and F420-reducing hydrogenase complex, both of which are required for the oxidation of the methyl groups to CO2 via the WLP [12]. This suggests that the “Ca. Methylarchaeales” cannot utilize the methylotrophic pathway for methanogenesis. Similar to methyl-reducing methanogens of the Methanonatronarchaeales [17], function of the defective WLP remains a mystery.The “Ca. Methylarchaeales” MAGs contain one or two copies of a gene encoding heterodisulfide reductase subunit D (HdrD) (Supplementary Fig. 7 and Supplementary Table 7), one of which was co-located with a b-type cytochrome gene (Fig. 3a and Supplementary Fig. 7), which is similar to the hdrDE operon of Methanosarcina barkeri [25]. The b-type cytochromes in the HdrDE-like complex of the “Ca. Methylarchaeales” are integral membrane proteins with five transmembrane helical segments that harbor a nitrate reductase gamma subunit domain (PF02665) (Fig. 3c and Supplementary Figs. 7 and 8). Sequence analysis of these b-type cytochromes revealed two histidine residues located in Helix 2 of these proteins in all the “Ca. Methylarchaeales” genomes, two histidine residues located in Helix 5 for H03B1, and single histidine and methionine residues located in Helix 5 for “Ca. Methanotowutia” and “Ca. Methanoinsularis” (Supplementary Fig. 7b and Fig. 3c). These residues are suggested to be involved in the binding of two heme groups [26], similar to the NarI of E. coli [27] and HdrE of M. barkeri [25]. It is assumed that the two heme groups ligated to histidine or methionine residues of Helix 1 and Helix 5 are on the periplasmic and cytoplasmic side of the membrane bilayer respectively, and are responsible for electron transfer. In addition, the hdrDE operon is adjacent to the mcrABDG operon in all the “Ca. Methylarchaeales” MAGS (Fig. 3a), supporting their role in methanogenesis for these microorganisms. Collectively, these findings strongly indicate that members of the “Ca. Methylarchaeales” are b-type cytochrome-containing methanogens that use the HdrDE complex to reduce the heterodisulfide CoM-S-S-CoB of Coenzymes M and B generated in the final step of methanogenesis [28] (Fig. 2).Fig. 3: Gene composition and structural model of HdrDE and VhtAGC complexes in the “Ca. Methylarchaeales”.a Gene composition of contigs/scaffolds containing the gene cluster of heterodisulfide reductase (HdrDE) complex. Genes related to methane metabolism are highlighted with red, blue, yellow, and cyan. The hdrDE complex gene cluster is always adjacent to mcrABDG operon. b Gene composition of methanophenazine-reducing hydrogenase (VhtAGC) complex. Genes for VhtAGC were collocated on the same contig/scaffold, forming a transcriptional unit. c Structural model of b-type cytochromes in HdrDE and VhtAGC complexes showing the proposed heme ligation.Full size imageWe identified a homolog of a 11-subunit NADH-quinone oxidoreductase complex in each “Ca. Methylarchaeales” genome (Supplementary Table 7) whose gene cluster resembles to the F420H2 dehydrogenase (Fpo) found in Methanosarcina [29] (Supplementary Fig. 9b). Phylogenetic analysis of the large subunit revealed that the “Ca. Methylarchaeales” complex is more closely related to the Fpo and Fpo-like complexes of Methanosarcinales and Methanomassiliicoccales than to group 4 [NiFe] hydrogenases (Supplementary Fig. 10). The absence of the typical [NiFe]-binding motifs in the catalytic subunit excludes the possibility that the complex is a group 4 [NiFe] hydrogenase (Supplementary Fig. 9a). In addition, the complex also lack the FpoF subunit required for binding and oxidation of F420H2 [15]. This suggests that this Fpo-like complex is unable to interact with F420H2, and instead may use reduced ferredoxin as an electron donor, similar to its proposed role for the Methanomassiliicoccales [15] and Methanosaeta thermophila [30]. In six MAGs from “Ca. Methanoinsularis”, “Ca. Methanoporticola”, and “Ca. M. tengchongensis”, genes for soluble methyl viologen-reducing hydrogenase/heterodisulfide reductase complex (MvhADG/HdrABC) and methanophenazine-reducing hydrogenase complex (VhtAGC) are missing. It is extremely unlikely that genes encoding all MvhADG/HdrABC and VhtAGC complex subunits are present in these near-complete genomes but were missed by sequencing. Thus, it is proposed that these microorganisms may use the Fpo-like complex directly to accept electrons from reduced ferredoxin, and subsequently channel these electrons to the HdrDE complex coupled to the reduction of CoM-S-S-CoB (Fig. 2), as shown previously for Methanosaeta thermophila [30]. The reduced ferredoxin may be produced by some unidentified hydrogenases or an unknown pathway. The H03B1 MAG also encodes a formate dehydrogenase subunit A gene (fdhA) co-located with a fdhB gene (Supplementary Table 7) and a putative b-type cytochrome with five transmembrane helices and a prokaryotic b561 domain (PF01292) binding two heme groups (Supplementary Fig. 11c) that is similar to FdhC of E. coli. “Ca. M. tengchongensis” contained fdhAB genes, with the fdhB gene collocated with a gene for a cytochrome b561 with four transmembrane helices and two heme groups (Supplementary Fig. 11b). It is likely that these microorganisms may be able to use formate dehydrogenase to reduce methanophenazine pool which could then transfer electrons to the membrane-bound HdrDE complex (Fig. 2). We identified a geranylfarnesyl diphosphate synthase homolog in each “Ca. Methylarchaeales” genome. Phylogenetic analysis revealed that these enzymes cluster together with the geranylfarnesyl diphosphate synthase of M. mazei, likely suggesting that the “Ca. Methylarchaeales” may be able to synthesize methanophenazine, as previously shown in M. mazei [31] (Supplementary Fig. 12).The “Ca. Methanotowutia” (TDP8 and TDP10) MAGs encode the small and large subunits for a [NiFe] active site-containing hydrogenase co-located with a gene for membrane-spanning b561 domain (PF01292) cytochrome b (Fig. 3b), which is similar to the operon of VhtAGC complex found in Methanosarcina with cytochromes [12]. The b-type cytochrome harbors five transmembrane helices, with histidine or methionine residues located in Helix 1, 2, 5 for the ligation of two heme groups (Supplementary Fig. 11a). It has been proposed that the VhtA is guided to the cell membrane with the help of twin-arginine signal peptide of VhtG and its [NiFe] active site faces periplasmic side [32, 33]. As a result, two H+ ions generated by H2 oxidation are released into the periplasm while two electrons are transferred to heme groups of VhtC through Fe-S clusters of VhtG [12, 34]. Furthermore, the electron carrier methanophenazine connects VhtAGC with HdrDE, and its reduction and reoxidation results in the release of two additional H+ ions into the periplasm (Fig. 2) [34, 35]. Altogether, four electrogenic protons are generated in the system, which can be used to drive the synthesis of one ATP via an archaeal A-type ATP synthase. The HdrDE complex that receives electrons from the methanophenazine can be used to reduce CoM-S-S-CoB (Fig. 2), enabling the coupling of methane production with energy conservation. This is the first report of a VhtAGC complex and an HdrDE complex found in an mcr-containing archaeal lineage outside the Euryarchaeota superphylum (Fig. 1) and indicates that “Ca. Methanotowutia” may be capable of performing H2-dependent methyl-reducing methanogenesis. The membrane-bound electron transport chain is more efficient than electron bifurcation that is used by methanogens without cytochromes [12].Sequence analysis revealed that key conserved residues of the McrA sequences of the “Ca. Methylarchaeales”, including the binding sites for F430 cofactors, coenzyme M, and coenzyme B [36], are the same as those in McrA sequences of members of the Euryarchaeota superphylum, with exception that the cysteine at site α452 is replaced with an alanine or serine (Supplementary Fig. 13 and Supplementary Table 8). Phylogenetic trees of concatenated and individual McrABG were reconstructed, showing that the “Ca. Methylarchaeales” encode canonical Mcr complexes that cluster with those of putative methane-metabolizing archaea and are divergent from those of short-chain alkane-oxidizing archaea (Fig. 4 and Supplementary Fig. 14). These results support the view that the “Ca. Methylarchaeales” metabolize methane.Fig. 4: Phylogeny of the Mcr/Mcr-like complex showing the relationship with their species tree.a Maximum-likelihood tree (IQ-TREE, LG + C60 + F + G) based on an alignment of concatenated McrABG/McrABG-like subunits from 167 archaeal genomes. The Mcr-like complex is found in short-chain alkane-oxidizing archaea. b Maximum-likelihood tree (IQTREE, LG + C60 + F + G) based on concatenated 122 archaeal-specific marker proteins using the same genomes with those of Mcr/Mcr-like tree. Ultrafast bootstraps values ≥95 are indicated with green filled squares.Full size imageWe also explored the possibility that the “Ca. Methylarchaeales” may be able to oxidize methane. In reported anaerobic methanotrophic archaea (ANME), methane oxidation is coupled to the reduction of several electron acceptors (nitrate, sulfate or metal oxides). Known ANME are predicted to utilize canonical terminal respiratory reductases or multi-heme c-type cytochromes (MHCs) to transfer electrons to a syntrophic partner microorganism [37], metal oxides [38, 39] or humics [40]. We could not identify any terminal reductases or MHCs in the “Ca. Methylarchaeales” genomes. Previous studies have hypothesized that formate or acetate might act as potential syntrophic electron carriers between methane-oxidizing archaea and their partners [41, 42], and members of the “Ca. Methylarchaeales” possesses the genetic potential for the production of these electron carriers. However, to our knowledge, these electron-transferring mechanisms have never been experimentally verified for ANME. Collectively, these analyses suggest that these “Ca. Methylarchaeales” are more likely methanogens, although empirical studies are required to confirm this.Similar to all described methanogens [15], the “Ca. Methylarchaeales” do not encode a complete tricarboxylic acid cycle, with citrate synthase, fumarase and succinate dehydrogenase absent from these MAGs. The “Ca. Methylarchaeales” lack a canonical pyruvate kinase for glycolysis (Supplementary Fig. 15 and Supplementary Table 7). However, pyruvate-water dikinase or pyruvate phosphate dikinase in gluconeogenesis may replace pyruvate kinase to catalyze the reversible interconversion of phosphoenolpyruvate and pyruvate, as shown in cultivated methanogens Methanomassiliicoccales [15]. The identification of sugar transport proteins and a variety of extracellular and intracellular carbohydrate-active enzymes (CAZymes) including glycoside hydrolases (EC 3.2.1.1 and 5.4.99.16) and glycosyltransferases (EC 2.4.1, 2.4.1.83, and 2.4.99.18, etc.) in the “Ca. Methylarchaeales” (Supplementary Fig. 15) suggests that they may be able to utilize sugars as an alternative carbon and energy source, as previously hypothesized for the “Ca. Methanomethylicales” and “Ca. Bathyarchaeia” [4, 8]. However, comparative genomics revealed that cultured methanogens that do not utilize sugars also encode similar proteins (Supplementary Fig. 15) [12, 13], and they may instead be involved in biosynthetic pathways. In addition, peptide and amino acid transporters, and enzymes related to peptide fermentation including extracellular peptidases, endopeptidases, 2-oxoglutarate ferredoxin oxidoreductase (kor), 2-ketoisovalerate ferredoxin oxidoreductase (vor), indolepyruvate ferredoxin oxidoreductase (ior), and pyruvate ferredoxin oxidoreductase (por) are present in both the “Ca. Methylarchaeales” and cultured methanogens (Supplementary Fig. 15). Nevertheless, to our best knowledge, peptide fermentation has never been reported in these isolated methanogens to date. Thus, the genes may be involved in assimilation and metabolism of amino acids in the “Ca. Methylarchaeales” and other newly discovered uncultured methanogens [4, 8, 12].Evolution of the b-type cytochrome-containing methanogensThe rapid increase in the number and diversity of MAGs has greatly expanded the known diversity and distribution of Mcr genes in archaea. To investigate the evolutionary history of the Mcr complexes in methanogens, we inferred the phylogeny of concatenated McrABG subunits based on all mcr-containing archaeal genomes available in public databases. In accordance with previous studies [43, 44], lineages in Class I and Class II methanogens within the Euryarchaeota superphylum appear congruent between McrABG and species trees while H2-dependent methylotrophic methanogens Methanomassiliicoccales and Methanonatronarchaeia, and methanotroph “Ca. Methanophagales” (ANME-1) are not (Fig. 4). The results were further supported by the phylogeny of the six conserved markers (m4–m9) in this (Supplementary Fig. 16) and previous studies [44]. These markers are solely present in archaea containing Mcr or Mcr-like complexes and suggested to be involved in activation, folding and assembly of Mcr subunits [44]. The Mcr genes of “Ca. Methanomethylicales” and “Ca. Korarchaeia” within the phylum Thermoproteota were previously suggested to be acquired via HGTs, since they are closely related with those of methylotrophic methanogens of the Euryarchaeota superphylum in McrABG tree [44]. However, analyses including our “Ca. Methylarchaeales” MAGs and several others with an Mcr complex revealed good congruence between the concatenated McrABG, m4-m9 genes, and the genome-based trees for the lineages within the Thermoproteota (including the “Ca. Methanomethylicales”, “Ca. Korarchaeia”, “Ca. Nezhaarchaeales”, and our “Ca. Methylarchaeales”; Fig. 4 and Supplementary Fig. 16) support vertical inheritance and evolution independent of the Euryarchaeota superphylum. Wide distribution of mcr genes in archaea (Supplementary Fig. 17 and Supplementary Table 9) and their congruence with the genome-based tree for many lineages within the Euryarchaeota superphylum and the Thermoproteota suggest that these genes likely have originated before the divergence of these two major archaeal lineages.Recently, amalgamated likelihood estimation (ALE) has been used to estimate presence probability of McrA in each internal node in a rooted archaeal species tree, supporting the presence of McrA with high confidence in the common ancestor of Class I and Class II methanogens, “Ca. Methanofastidiosales”/“Ca. Nuwarchaeales” in Euryarchaeota superphylum, as well as “Ca. Methanomethylicales”, “Ca. Korarchaeia”, and “Ca. Nezhaarchaeales” in the Thermoproteota [45]. Compared to the previous study [45], our ALE results support the presence of McrA with high confidence [presence probability (pp) >0.9] at the basal node of “Ca. Methanomethylicales”, “Ca. Nezhaarchaeales”, “Ca. Korarchaeia”, and “Ca. Methylarchaeales” in the Thermoproteota (Supplementary Fig. 17), suggesting an earlier origin of Mcr complex in Thermoproteota. The difference is likely attributed to the addition of “Ca. Methylarchaeales”. Confidence in evolutionary inferences from ALE analyses will require expansion of genome coverage of some of the poorly represented or yet-to-be-discovered Mcr-containing lineages. A previous study showed that an ancestral McrA sequence were more closely related to McrA from “Ca. Methanodesulfokores washburnensis” in the “Ca. Korarchaeia” compared to any other lineages [6], possibly supporting our inference that methane metabolism may have evolved relatively early in Thermoproteota.The b-type cytochrome in HdrDE complex belongs to the protein family of nitrate reductase gamma subunit (PF02665, NarI). Using all publicly available archaeal genomes, we found that the NarI domain-containing cytochromes (NarI-Cyt) are primarily used in three electron transfer complexes: HdrDE, dissimilatory nitrate reductase (NarGHI) [46], and sulfite reductase (DsrABCJKMOP). For the HdrDE and NarGHI complexes, the genes encoding the subunits are co-localized in archaeal genomes, each forming a transcriptional unit. However, in the Dsr complex, only a DsrK is co-localized with a DsrM (b-type cytochrome) while other subunits are usually not adjacent to the DsrKM but separated by few genes [6]. We examined distribution of the three complexes in archaea. A total of 101 genomes were found to encode these complexes (66 for HdrDE, 16 for Nar, 23 for Dsr), and they are distributed across the Euryarchaeota superphylum, Thermoproteota, and Asgardarchaeota (Supplementary Fig. 17 and Supplementary Table 9). Among these genomes, the HdrDE is found in methanogens and methanotrophs belonging to the class “Ca. Methanosarcinia”, the orders Methanomicrobiales and Methanonatronarchaeales, and in alkane-oxidizing archaea belonging to the orders Archaeoglobales, “Ca. Syntropharchaeales”, and Methanosarcinales (GoM-Arc1) (Supplementary Fig. 17). In Mcr-containing archaea outside of the Euryarchaeota superphylum, the complex is exclusively found in the “Ca. Methylarchaeales” (Fig. 1 and Supplementary Fig. 17).Phylogenetic analyses of the NarI-Cyt were conducted to investigate the evolution of these genes in archaea (Fig. 5a). The results showed that these cytochromes have experienced frequent horizontal gene transfer, especially DsrM. The DsrM sequences annotated in members of the Thermoproteota form a distinct cluster. In the cluster, Archaeoglobi and “Ca. Hydrothermarchaeota” DsrM branch far from their Euryarchaeota superphylum relatives, and have potentially gained their cytochromes from a member of the “Ca. Korarchaeia”. Similarly, the “Ca. Methanoperedenaceae” and Archaeoglobi might have acquired their NarI genes from a member of Thermoproteia. Congruence between the cytochrome and genome-based trees for members of the Thermoproteota suggest that these cytochromes might have evolved before the diversification of this phylum. We further inferred a gene tree using concatenated HdrDE complex (Fig. 5b). The topological structure of this tree exhibits high congruence with the genome-based tree for all lineages except the Methanonatronarchaeia, supporting an early presence of the complex in archaea. This suggestion is supported by ALE analyses which indicate the presence of NarI-Cyt with high confidence in the common ancestor of Thermoproteota (pp = 0.69) and in the common ancestor of “Ca. Halobacteriota” (pp = 0.70) (Supplementary Fig. 17).Fig. 5: Phylogeny of NarI-domain-containing b-type cytochromes and concatenated HdrDE complexes in archaea.a Phylogeny of NarI-domain-containing b-type cytochromes in archaea. b Phylogeny of concatenated HdrDE complexes in archaea. The maximum-likelihood trees of NarI-domain-containing b-type cytochromes (a (a’)) and concatenated HdrDE subunits (b (a’)) from representative archaea are inferred with IQ-TREE (LG + C60 + F + G, -bb: 10,000 for NarI-domain, 1000 for HdrDE). The b-type cytochromes comprising different enzyme complexes are indicated by different color dots (light red for HdrE, yellow for DsrM, and blue for NarI). HdrE heterodisulfide reductase E subunit, DsrM sulfite reductase M subunit, NarI dissimilatory nitrate reductase I subunit. The maximum-likelihood trees of a concatenated set of 122 archaeal-specific marker proteins using the same genomes as those of NarI-domain-containing b-type cytochrome tree (a (b’)) and HdrDE complexe tree (b (b’)), respectively. The trees were computed with IQ-TREE using LG + C60 + F + G model. These genomes or clades with Mcr complexes are marked by pink dots. The bootstrap support values ≥95 are indicated with green filled squares.Full size imageAs mentioned above, b-type cytochromes are classified into different protein families, and form part of many membrane-bound electron transfer complexes in bioenergetic pathways [47, 48]. Aside from HdrDE, Nar, and Dsr, such complexes also include Vht, Fdh, b6f complex, bc1 complex, and succinate dehydrogenase (Sdh). We examined the distribution of different families of b-type cytochromes in 416 representative archaea covering 41 orders or phyla of the Euryarchaeota superphylum, Thermoproteota, and Asgardarchaeota (Supplementary Fig. 17 and Supplementary Table 9). A total of 246 genomes contained these b-type cytochromes that were distributed across 23 archaeal lineages. In total, 11 of the 13 lineages of the Thermoproteota, and 11 of the 24 orders in Euryarchaeota superphylum, had b-type cytochrome, suggesting its pervasiveness in archaea. We conducted phylogenetic analyses of the b-type cytochromes from different families (Fig. 6a). The result indicates that cytochromes from Fdh and Sdh complexes form two large clusters. Within each cluster, lineages from Thermoproteota or the Euryarchaeota superphylum were essentially grouped together, suggesting that these cytochromes may have evolved before the divergence of these major archaeal lineages. The cluster of cytochromes of the b6f complex is close to those of the bc1 complex, consistent with the suggestion that bacterial cytochromes in bc1 complex might originate from cytochromes in b6f complex [48]. A phylogenetic analysis of concatenated VhtAGC showed clustering of lineages from Thermoproteota with Archaeoglobi (Fig. 6b), suggesting ancient exchanges of the Vht complex among these lineages. Taken together, these results support an early origin of b-type cytochromes in archaea. Previous studies also imply that some core enzymes for bioenergetic pathways, including membrane-integral b-type cytochrome, formate dehydrogenase, [NiFe]-hydrogenase, the Rieske/cytb complexes, and NO-reductases, were present in the Last Universal Common Ancestor of Bacteria and Archaea [48, 49].Fig. 6: Phylogeny of b-type cytochromes and concatenated VhtAGC complexes in archaea.a Maximum-likelihood tree of b-type cytochromes of representative archaea (NarI-domain-containing b-type cytochromes not included) inferred using IQ-TREE (the best model: cpREV + F + G4). Different families of b-type cytochromes are shown. vht methanophenazine-reducing hydrogenase complex, fdh formate dehydrogenase, sdh succinate dehydrogenase. b Maximum-likelihood tree of concatenated VhtAGC subunits retrieved from representative archaea, inferred with IQ-TREE using LG + C60 + F + G model. The bootstrap support values ≥95 are indicated with filled squares. Genomes or clades with Mcr complexes are marked by green filled dots. The number of sequences for branches is given in parenthesis. The pink branches represent members of Thermoproteota phylum while the black branches represent members of Euryarchaeota superphylum.Full size imageAs the heme is indispensable to b-type cytochrome [47], we also investigated distribution of its biosynthetic pathway in archaea. Although there are 11 genes involving in the heme biosynthesis, the three genes (Ahb-NirDH, Ahb-NirJ1, and Ahb-NirJ2), responsible for conversion from precorrin-2 to heme, are the key to this pathway. Thus, these three genes were used as markers denoting the presence of heme biosynthetic pathway. Among 41 archaeal lineages, 32 had this pathway including the “Ca. Methylarchaeales” (Supplemental text, Fig. 2, Supplementary Fig. 17 and Supplementary Table 9). Phylogenetic analyses reveal that these lineages from Thermoproteota largely cluster together for Ahb-NirDH (Supplementary Fig. 18). However, for Ahb-NirJ1 and Ahb-NirJ2, lineages from the Euryarchaeota superphylum, the Thermoproteota, and Asgardarchaeota are tangled up, suggesting frequent HGTs of these genes between these lineages. The wide distribution of this pathway across the Euryarchaeota superphylum, the Thermoproteota, and Asgardarchaeota (Supplementary Fig. 17 and Supplementary Table 9) suggests that a common ancestor may have been able to synthesize heme. This observation further supports the possibility of the early presence of b-type cytochromes in archaea.Here we described the discovery of the novel archaeal order “Ca. Methylarchaeales”, expanding known methanogen and archaeal diversity. Members of the lineage are methyl-reducing methanogens that can conserve energy via membrane-bound electron transport chains. The “Ca. Methylarchaeales” are globally distributed in anoxic lake and marine sediments, suggesting that they make an important contribution to global methane emissions. Our broader analyses suggest that methanogens who use b-type cytochrome-containing complexes to transfer electrons may have originated before diversification of Thermoproteota or “Ca. Halobacteriota” phyla based on a conservative estimation for the origin of McrA and NarI-Cyt genes in the ALE analysis. A previous study using molecular clock analyses to indicate that the diversification of Thermoproteota likely occurred in the early Archean Eon [45]. Archean oceans are thought to have been anoxic and contain abundant ferrous iron from hydrothermal volcanics [50, 51], which would have provided sufficient raw materials for heme synthesis by methanogens. In addition, CO2, H2, and organic compounds produced by volcanic activity are transported to the early oceans [52], which provides adequate carbon and energy sources for methanogenic growth. Compared to hydrogenotrophic methanogens using electron bifurcation, methanogens using the membrane-bound electron chain have a higher energy production efficiency and growth yield, providing an advantage for members of the “Ca. Methylarchaeales” described here.Taxonomic proposals“Ca. Methanotowutia igneaquae” (gen. nov., sp. nov.)Methanotowutia (Me.tha.no.to.wu’ti.a. N.L. pref. methano-, pertaining to methane; N.L. fem. n. Methanotowutia methanogenic organism named after the lake Towuti in Indonesia where members of the genus were first discovered).Methanotowutia igneaquae (ig.ne.a’quae. L. masc. adj. igneus, of fire; L. fem. n. aqua, freshwater, pertaining to freshwater habitats; N.L. gen. n. igneaquae from/of water of fire, referring to the volcanic lake environment). This organism is deduced to be able to use methylated compounds for methanogenesis. Representative genomes are near-complete bins TDP8 (Accession No. SAMN15658089) and TDP10 (Accession No. SAMN15658091) recovered from freshwater sediments in Lake Towuti in Indonesia with the latter the type genome for the species.“Ca. Methanoinsularis halodrymi” (gen. nov., sp. nov.)Methanoinsularis (Me.tha.no.in.su.la’ris. N.L. pref. methano-, pertaining to methane; L. fem. adj. insularis, from an island; N.L. fem. n. Methanoinsularis methanogenic organism from an island, specifically referring to Techeng Island in China where these microorganisms were discovered).Methanoinsularis halodrymi (ha.lo.dry’mi. Gr. masc. n. hals (gen. halos) salt; Gr. masc. n. drymos coppice; N.L. gen. n. halodrymi of salty woodland, referring to the mangrove wetland environment). This uncultivated microorganism is assumed to be able to perform methylotrophic methanogenesis. The type genome for the species is the bin H03B1 (Accession No. SAMN15658086) recovered from mangrove wetlands in Techeng Island in China.“Ca. Methanoinsularis haikouensis” (gen. nov., sp. nov.)Methanoinsularis haikouensis (hai.kou.en’sis. N.L. fem. adj. haikouensis, pertaining to Haikou). This uncultivated microorganism is assumed to be able to perform methylotrophic methanogenesis. Representative genomes are the bins HK01M, HK01B, HK02M1 (Accession No. SAMN25131447, SAMN25131448, SAMN25131449) recovered from mangrove wetlands in Dongzhai Harbour in Haikou, China.“Ca. Methanoporticola haikouensis” (gen. nov., sp. nov.)Methanoporticola (Me.tha.no.por.ti’co.la. N.L. pref. methano-, pertaining to methane; L. masc. n. portus, harbour; L. suff. -cola (from L. masc. or fem. n. incola), inhabitant, dweller; N.L. masc. n. Methanoporticol, a methane-forming dweller of a harbor, specifically referring to Dongzhai Harbour in China where these microorganisms were discovered).Methanoporticola haikouensis (hai.kou.en’sis. N.L. masc. adj. haikouensis, pertaining to Haikou). This uncultivated microorganism is assumed to be able to perform methylotrophic methanogenesis. The type genome for the species is the bin HK02M2 (Accession No. SAMN25131450) recovered from mangrove wetlands in Dongzhai Harbour in Haikou, China.“Ca. Methylarchaeales” (ord. nov.)Methylarchaeales (Me.thyl.ar.cha.ea’les. N.L. neut. n. Methylarchaeum (Candidatus) type genus of the order; -ales, ending denoting an order; N.L. fem. pl. n. Methylarchaeales, the order of the genus “Ca. Methylarchaeum”); Methylarchaeaceae (Me.thyl.ar.chae.a.ce’ae. N.L. neut. n. Methylarchaeum (Candidatus) type genus of the family); -aceae, ending denoting a family; N.L. fem. pl. n. Methylarchaeaceae, the family of the genus “Ca. Methylarchaeum”). More

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    Effects of cavity orientation on nesting success inferred from long-term monitoring of the endangered red-cockaded woodpecker

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