Core Metabolic Features and Hot Origin of Bathyarchaeota

The archaeal phylum Bathyarchaeota comprises highly diversified subgroups and is considered to be one of the most abundant microorganisms on earth. The metabolic features and evolution of this phylum still remain largely unknown. In this article, a comparative metabolic analysis of 15 newly reconstructed and 36 published metagenomic assembled genomes (MAGs) spanning 10 subgroups was performed, revealing the core metabolic features of Bathyarchaeota—namely, protein, lipid, and benzoate degradation;glycolysis;and the Wood–Ljungdahl (WL) pathway, indicating an acetyl-CoA-centralized metabolism within this phylum. Furthermore, a partial tricarboxylic acid (TCA) cycle, acetogenesis, and sulfur-related metabolic pathways were found in specific subgroups, suggesting versatile metabolic capabilities and ecological functions of different subgroups. Intriguingly, most of the MAGs from the Bathy-21 and -22 subgroups, which are placed at the phylogenetic root of all bathyarchaeotal lineages and likely represent the ancient Bathyarchaeota types, were found in hydrothermal environments and encoded reverse gyrase, suggesting a hyperthermophilic feature. This work reveals the core metabolic features of Bathyarchaeota, and indicates a hot origin of this archaeal phylum.

早寒武纪清江丝菌牵出硫酸盐还原菌与地球环境协同演化 历史

Sulfate reduction is an essential metabolism that maintains biogeochemical cycles in marine and terrestrial ecosystems.Sulfate reducers are exclusively prokaryotic,phylogenetically diverse,and may have evolved early in Earth’s history.However,their origin is elusive and unequivocal fossils are lacking.Here we report a new microfossil,Qingjiangonema cambria,from518-million-year-old black shales that yield the Qingjiang biota.Qingjiangonema is a long filamentous form comprising hundreds of cells filled by equimorphic and equidimensional pyrite microcrystals with a light sulfur isotope composition.Multiple lines of evidence indicate Qingjiangonema was a sulfate-reducing bacterium that exhibits similar patterns of cell organization to filamentous forms within the phylum Desulfobacterota,including the sulfate-reducing Desulfonema and sulfide-oxidizing cable bacteria.Phylogenomic analyses confirm separate,independent origins of multicellularity in Desulfonema and in cable bacteria.Molecular clock analyses infer that the Desulfobacterota,which encompass a majority of sulfate-reducing taxa,diverged~2.41 billion years ago during the Paleoproterozoic Great Oxygenation Event,while cable bacteria diverged~0.56 billion years ago during or immediately after the Neoproterozoic Oxygenation Event.Taken together,we interpret Qingjiangonema as a multicellular sulfate-reducing microfossil and propose that cable bacteria evolved from a multicellular filamentous sulfate-reducing ancestor.We infer that the diversification of the Desulfobacterota and the origin of cable bacteria may have been responses to oxygenation events in Earth’s history.

Widespread Bathyarchaeia encode a novel methyltransferase utilizing lignin-derived aromatics

Lignin degradation is a major process in the global carbon cycle across both terrestrial and marine ecosystems.Bathyarchaeia,which are among the most abundant microorganisms in marine sediment,have been proposed to mediate anaerobic lignin degradation.However,the mechanism of bathyarchaeial lignin degradation remains unclear.Here,we report an enrichment culture of Bathy-archaeia,named Candidatus Baizosediminiarchaeum ligniniphilus DL1YTT001(Ca.B.ligniniphilus),from coastal sediments that can grow with lignin as the sole organic carbon source under mesophilic anoxic conditions.Ca.B.ligniniphilus possesses and highly expresses novel methyltransferase 1(MT1,mtgB)for transferring methoxyl groups from lignin monomers to cob(I)alamin.MtgBs have no homology with known microbial methyltransferases and are present only in bathyarchaeial lineages.Heterologous expression of the mtgB gene confirmed O-demethylation activity.The mtgB genes were identified in metagenomic data sets from a wide range of coastal sediments,and they were highly expressed in coastal sediments from the East China Sea.These findings suggest that Bathyarchaeia,capable of O-demethylation via their novel and specific methyltransferases,are ubiquitous in coastal sediments.

Metal-dependent anaerobic methane oxidation in marine sediment:insights from marine settings and other systems

Anaerobic oxidation of methane(AOM) plays a crucial role in controlling global methane emission. This is a microbial process that relies on the reduction of external electron acceptors such as sulfate, nitrate/nitrite, and transient metal ions. In marine settings, the dominant electron acceptor for AOM is sulfate, while other known electron acceptors are transient metal ions such as iron and manganese oxides. Despite the AOM process coupled with sulfate reduction being relatively well characterized,researches on metal-dependent AOM process are few, and no microorganism has to date been identified as being responsible for this reaction in natural marine environments. In this review, geochemical evidences of metal-dependent AOM from sediment cores in various marine environments are summarized. Studies have showed that iron and manganese are reduced in accordance with methane oxidation in seeps or diffusive profiles below the methanogenesis zone. The potential biochemical basis and mechanisms for metal-dependent AOM processes are here presented and discussed. Future research will shed light on the microbes involved in this process and also on the molecular basis of the electron transfer between these microbes and metals in natural marine environments.

The late Archaean to early Proterozoic origin and evolution of anaerobic methane-oxidizing archaea

Impact statement Microorganisms,called anaerobic methane-oxidizing archaea(ANME),can reduce a large amount of greenhouse gas methane and therefore have the potential to cool the Earth.We collected nearly all ANMEs genomes in public databases and performed a comprehensive comparative genomic analysis and molecular dating.Our results show that ANMEs originated in the late Archaean to early Proterozoic eon.During this period of time,our planet Earth was experiencing the Great Oxygenation Event and Huronian Glaciation,a dramatic drop in the Earth's surface temperature.This suggests that the emergence of ANMEs may contribute to the reduction of methane at that time,which is an unappreciated potential cause that led to the Huronian Glaciation.

New approaches for archaeal genome-guided cultivation

Archaea,one of the three domains of life along with Bacteria and Eukarya,contains ancient life forms such as methanogen that are observed today on Earth,and one lineage Asgard archaea is also considered the closest ancestor of Eukarya.Recently,with the development of interdisciplinary studies from Earth and Life sciences,archaeal organisms are considered to play pivotal roles in geochemical cycling in nature.However,our understanding of the attributes,origin and evolution,geochemical and ecological functions of Archaea is hampered by the scarcity of archaeal isolates,which has represented a challenge to researchers for the last 40 years.Cultivation-independent sequencing and phylogenomic analyses have demonstrated a considerable diversity of Archaea with more than 20 novel phyla.However,only four archaeal phyla have cultured representatives,leaving large gaps in our knowledge of the metabolic capabilities and ecological functions of the majority of archaeal strains identified exclusively by DNA sequencing.In this review,we summarize the discovery and development of archaeal research,highlight the knowledge gap between uncultured and cultured archaeal microbes,and call on the importance of devoting greater research efforts to archaeal cultivation.Finally,we outlined new ideas and strategic approaches,namely,(1)genome-based methods,(2)microbial network information-based methods,(3)genome-scale model-guided methods,and(4)machine learning methods,to enable the cultivation of uncultivated archaeal microbes using accumulated high-throughput sequencing data.

Expanding Asgard members in the domain of Archaea sheds new light on the origin of eukaryotes

The hypothesis that eukaryotes originated from within the domain Archaea has been strongly supported by recent phylogenomic analyses placing Heimdallarchaeota-Wukongarchaeota branch from the Asgard superphylum as the closest known archaeal sister-group to eukaryotes. However, our understanding is still limited in terms of the relationship between eukaryotes and archaea, as well as the evolution and ecological functions of the Asgard archaea. Here, we describe three previously unknown phylum-level Asgard archaeal lineages, tentatively named Sigyn-, Freyr-and Njordarchaeota. Additional members in Wukongarchaeota and Baldrarchaeota from distinct environments are also reported here, further expanding their ecological roles and metabolic capacities. Comprehensive phylogenomic analyses further supported the origin of eukaryotes within Asgard archaea and a new lineage Njordarchaeota was supposed as the known closest branch with the eukaryotic nuclear host lineage. Metabolic reconstruction suggests that Njordarchaeota may have a heterotrophic lifestyle with capability of peptides and amino acids utilization, while Sigynarchaeota and Freyrarchaeota also have the potentials to fix inorganic carbon via the Wood-Ljungdahl pathway and degrade organic matters. Additionally, the Ack/Pta pathway for homoacetogenesis and de novo anaerobic cobalamin biosynthesis pathway were found in Freyrarchaeota and Wukongrarchaeota,respectively. Some previously unidentified eukaryotic signature proteins for intracellular membrane trafficking system, and the homologue of mu/sigma subunit of adaptor protein complex, were identified in Freyrarchaeota. This study expands the Asgard superphylum, sheds new light on the evolution of eukaryotes and improves our understanding of ecological functions of the Asgard archaea.