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De Anda, V.

Publications and source records attributed to De Anda, V..

12 recordsLinked to original sources

Archaeal lineages related to eukaryotes encode functional diterpenoid cyclases

The first eukaryotic cell originated through the union of an archaeon and a bacterium. Phylogenetic evidence suggests that the archaeal partner was a member of phylum Asgardarchaeota, likely within the Heimdallarchaeia clade. Although little is known about the molecular basis of eukaryogenesis, insight can be gained from studying the unique biochemistry of modern Asgardarchaeota. Here, we investigated the potential for Asgards to produce cyclic terpenoids. Phylogenomics coupled with structural prediction revealed that organisms from the clades Hodarchaeales and Kariarchaeaceae encode for diterpenoid cyclases. We tested the functionality of these enzymes in vitro, showing that they cyclize geranylgeranyl pyrophosphate to form bicyclic halimadienyl pyrophosphate. Halimadienyl nucleosides have previously been shown to mediate intracellular persistence of Mycobacterium tuberculosis in host endosomes, and may function similarly in Asgardarchaeota. The characterization of Asgard diterpenoid cyclases provides insight into the biochemistry of an elusive group of microbes that are pivotal in the evolution of complex cellular life.

microbiology↗

Genomic and proteomic characterization of sulfate-reducing symbionts of gutless marine annelids

Sulfate-reducing bacteria (SRB) are widespread in marine and terrestrial environments, where they often form syntrophic associations with bacteria, archaea, and eukaryotes. Among the most intimate of these are multipartite symbioses in gutless marine oligochaete worms, which host SRB and sulfur-oxidizing endosymbionts that engage in a syntrophic exchange of sulfur compounds. Despite decades of research on free-living SRB, the metabolic traits that enable SRB to persist in symbiosis, and how these differ across hosts and environments, remain poorly understood. Here, we show that a globally distributed clade of symbiotic SRB has a conserved core metabolism that diverges markedly from free-living relatives. Using comparative genomics and metaproteomics, we reveal that these endosymbionts retain key traits of SRB such as sulfate reduction, complete oxidation of acetate to CO2, amino acid degradation for nitrogen acquisition, and transport of essential nutrients. However, they exhibit a more oxygen-tolerant metabolism and lack typical nutrient-scavenging mechanisms of free-living SRB. One symbiont-specific trait, the glyoxylate bypass, was consistently expressed in situ and may serve both in reactive oxygen species defence and in biomass generation. The enrichment and expression of oxygen-tolerant pathways, coupled with the loss of nutrient-scavenging functions, indicate specialization to a host-associated, redox-fluctuating environment distinct from that of free-living SRB. Consistent with this shift, symbiont genomes are larger than those of free-living relatives, contrasting with genome reduction in many endosymbionts and reinforcing the importance of metabolic versatility. Our findings provide a framework for understanding how metabolic flexibility enables SRB to persist in long-term multipartite symbioses across diverse marine ecosystems.

microbiology↗

Methane production from hydrocarbons by consortia dominated by ANME archaea

Understanding microbial production and consumption of methane, a potent greenhouse gas in the atmosphere, is critical for bridging knowledge gaps in global carbon cycling. In anoxic environments, methane is known to be produced through hydrogenotrophic, acetoclastic or methylotrophic mechanisms. Methane production from hydrocarbons may also be important, especially in hydrocarbon-rich environments, like the Gulf of California, but the mechanism of this hydrocarbonoclastic methanogenesis remains unclear. The activity of consortia of anaerobic methane oxidizing (ANME) archaea and bacteria limits the release of methane to the atmosphere by consuming methane in anoxic environments globally. Here we used isotopic-labeling to track the conversion of hydrocarbons (hexadecane and naphthalene) to methane in enrichments from hydrothermally impacted, hydrocarbon-rich sediments from the Gulf of California. Methane was produced directly from hexadecane and naphthalene, in both the presence and absence of sulfate. We reconstructed metagenomic assembled-genomes (MAGs) from these experiments which revealed a mixture of bacteria dominated by Desulfobacteriota and Bacteroidota, and archaea dominated by Aeinigmarchaeota, Thermoplasmatota, and ANME group 2c. The ANME-2c were the only MAGs that encoded methyl coenzyme M reductases (McrA) and complete Wood-Ljungdahl pathways (WLP). This suggests that ANME-2c archaea may be involved in the production of methane along the seafloor, and that our understanding of the roles of these globally important microbes is not yet fully appreciated.

microbiology↗

Structure-based inference of eukaryotic complexity in Asgard archaea

Asgard archaea played a key role in the origin of the eukaryotic cell. While previous studies found that Asgard genomes encode diverse eukaryotic signature proteins (ESPs), representing homologs of proteins that play important roles in the complex organization of eukaryotic cells, the cellular characteristics and complexity of the Asgard archaeal ancestor of eukaryotes remain unclear. Here, we used de novo protein structure modeling and sensitive sequence similarity detection algorithms within an expanded Asgard archaeal genomic dataset to build a structural catalogue of the Asgard archaeal pangenome and identify 908 new isomorphic ESPs (iESPs), representing clusters of protein structures most similar to eukaryotic proteins and that likely underwent extensive sequence divergence. While most previously identified ESPs were involved in cellular processes and signaling, iESPs are enriched in information storage and processing functions, with several being potentially implicated in facilitating cellular complexity. By expanding the complement of eukaryotic proteins in Asgard archaea, this study indicates that the archaeal ancestor of eukaryotes was more complex than previously assumed.

evolutionary biology↗

Oxygen metabolism in descendants of the archaeal-eukaryotic ancestor

Asgard archaea were pivotal in the origin of complex cellular life. Hodarchaeales (Asgardarchaeota class Heimdallarchaeia) were recently shown to be the closest relatives of eukaryotes. However, limited sampling of these archaea constrains our understanding of their ecology and evolution1-3, including their anticipated role in eukaryogenesis. Here, we nearly double the number of Asgardarchaeota metagenome-assembled genomes (MAGs) to 869, including 136 new Heimdallarchaeia (49 Hodarchaeales) and several novel lineages. Examining global distribution revealed Hodarcheales are primarily found in coastal marine sediments. Detailed analysis of their metabolic capabilities revealed guilds of Heimdallarchaeia are distinct from other Asgardarchaeota. These archaea encode hallmarks of aerobic eukaryotes, including electron transport chain complexes (III and IV), biosynthesis of heme, and response to reactive oxygen species (ROS). The predicted structural architecture of Heimdallarchaeia membrane-bound hydrogenases includes additional Complex-I-like subunits potentially increasing the proton motive force and ATP synthesis. Heimdallarchaeia genomes encode CoxD, which regulates the electron transport chain (ETC) in eukaryotes. Thus, key hallmarks for aerobic respiration may have been present in the Asgard-eukaryotic ancestor. Moreover, we found that Heimdallarchaeia is present in a variety of oxic marine environments. This expanded diversity reveals these Archaea likely conferred energetic advantages during early stages of eukaryogenesis, fueling cellular complexity.

microbiology↗

Genetic elements and defense systems drive diversification and evolution in Asgard archaea

Asgard Archaea are of great interest as the progenitors of Eukaryotes, but little is known about the mobile genetic elements (MGEs) that may shape their ongoing evolution. Here, we describe MGEs that replicate in Atabeyarchaeia, wetland Asgard archaea phylum represented by two complete genomes. We used soil depth-resolved population metagenomic datasets to track 18 MGEs for which genome structures were defined and precise chromosome integration sites could be identified for confident host linkage. Additionally, we identified a complete 20.67 kilobase pair (kbp) circular plasmid (the first reported for Asgard archaea) and two groups of viruses linked to Atabeyarchaeia, via CRISPR spacer targeting. Closely related 40 kbp viruses possess a hypervariable genomic region encoding combinations of specific genes for small cysteine-rich proteins structurally similar to restriction-homing endonucleases. One 10.9 kbp circularizable plasmid-like MGE integrates genomically into an Atabeyarchaeia chromosome and has a 2.5 kbp circularizable element integrated within it. The 10.9 kbp MGE encodes a highly expressed methylase with a sequence specificity matching an active methylation motif identified by PacBio sequencing. Restriction-modification of Atabeyarchaeia differs from that of another coexisting Asgard archaea Freyarchaeia which has few identified MGEs but possesses diverse defense mechanisms, including DISARM and Hachiman not found in Atabeyarchaeia. Overall, defense systems and methylation mechanisms of Asgard archaea likely modulate their interactions with MGEs, and integration/excision and copy number variation of MGEs in turn enable host genetic versatility.

microbiology↗

Asgard archaea modulate potential methanogenesis substrates in wetland soil

The roles of Asgard archaea in eukaryogenesis and marine biogeochemical cycles are well studied, yet their contributions in soil ecosystems are unknown. Of particular interest are Asgard archaeal contributions to methane cycling in wetland soils. To investigate this, we reconstructed two complete genomes for soil-associated Atabeyarchaeia, a new Asgard lineage, and the first complete genome of Freyarchaeia, and defined their metabolism in situ. Metatranscriptomics highlights high expression of [NiFe]-hydrogenases, pyruvate oxidation and carbon fixation via the Wood-Ljungdahl pathway genes. Also highly expressed are genes encoding enzymes for amino acid metabolism, anaerobic aldehyde oxidation, hydrogen peroxide detoxification and glycerol and carbohydrate breakdown to acetate and formate. Overall, soil-associated Asgard archaea are predicted to be non-methanogenic acetogens, likely impacting reservoirs of substrates for methane production in terrestrial ecosystems. One-Sentence SummaryComplete genomes of Asgard archaea, coupled with metatranscriptomic data, indicate roles in production and consumption of carbon compounds that are known to serve as substrates for methane production in wetlands.

microbiology↗

Asgard archaea defense systems and their roles in the origin of immunity in eukaryotes

Immune systems are integral to survival against viral infection. Recently, dozens of new antiviral systems have been characterized in bacteria1. Some of these systems are present in eukaryotes and appear to have originated in prokaryotes. However, little is known about these defense mechanisms in archaea. Here, we identified 2,610 complete defense systems in archaea related to eukaryotes, the Asgardarchaeota2. These comprise 89 unique systems, including argonaute, NLR, mokosh, viperin, lassamu, and CBASS. Asgard viperin (asVip) and argonaute (asAgo) proteins are present at high frequencies compared to bacteria and have structural homology to eukaryotes. Phylogenetic analyses revealed asVips are ancestral eukaryotic proteins. Heterologous expression of asVips in bacteria, including the lineage closest to eukaryotes, Hodarchaeales, showed anti-phage activity. Eukaryotic- and bacterial-argonaute proteins appear to have originated in Asgardarchaeota and preserve ancient structural characteristics. asAgos have argonaute-PIWI domains which are key components of the RNA interference (RNAi) in eukaryotes. Characterization of hundreds of defense systems in the Asgardarchaeota revealed these archaea played important roles in the innovation of viral protection in eukaryotes. Given their relationship to eukaryotes, these defense systems may have applications in biomedicine and biotechnology.

microbiology↗

Unique viruses that infect Archaea related to eukaryotes

Asgard archaea are newly described microbes that are related to eukaryotes. Asgards are diverse and globally distributed, however, their viruses have not been described. Here we characterize seven viral genomes that infected Lokiarchaeota, Helarchaeota, and Thorarchaeota in deep-sea hydrothermal sediments. These viruses code for structural proteins similar to those in Caudovirales, as well as proteins distinct from those described in archaeal viruses. They also have genes common in eukaryotic nucleocytoplasmic large DNA viruses (NCLDVs), and are predicted to be capable of semi-autonomous genome replication, repair, epigenetic modifications, and transcriptional regulation. Moreover, Helarchaeota viruses may hijack host ubiquitin systems similar to eukaryotic viruses. This first glimpse of Asgard viruses reveals they have features of both prokaryotic and eukaryotic viruses, and provides insights into their roles in the ecology and evolution of these globally distributed microbes.

microbiology↗

Evolutionary history of dimethylsulfoniopropionate (DMSP) demethylation enzyme DmdA in marine bacteria

Dimethylsulfoniopropionate (DMSP), an osmolyte produced by oceanic phytoplankton, is predominantly degraded by bacteria belonging to the Roseobacter lineage and other marine Alphaproteobacteria via DMSP-dependent demethylase A protein (DmdA). To date, the evolutionary history of DmdA gene family is unclear. Some studies indicate a common ancestry between DmdA and GcvT gene families and a co-evolution between Roseobacter and the DMSP-producing-phytoplankton around 250 million years ago (Mya). In this work, we analyzed the evolution of DmdA under three possible evolutionary scenarios: 1) a recent common ancestor of DmdA and GcvT, 2) a coevolution between Roseobacter and the DMSP-producing-phytoplankton, and 3) pre-adapted enzymes to DMSP prior to Roseobacter origin. Our analyses indicate that DmdA is a new gene family originated from GcvT genes by duplication and functional divergence driven by positive selection before a coevolution between Roseobacter and phytoplankton. Our data suggest that Roseobacter acquired dmdA by horizontal gene transfer prior to exposition to an environment with higher DMSP. Here, we propose that the ancestor that carried the DMSP demethylation pathway genes evolved in the Archean, and was exposed to a higher concentration of DMSP in a sulfur rich atmosphere and anoxic ocean, compared to recent Roseobacter ecoparalogs (copies performing the same function under different conditions), which should be adapted to lower concentrations of DMSP.

evolutionary biology↗

MEBS, a software platform to evaluate large (meta)genomic collections according to their metabolic machinery: unraveling the sulfur cycle

BACKGROUNDThe increasing number of metagenomic and genomic sequences has dramatically improved our understanding of microbial diversity, yet our ability to infer metabolic capabilities in such datasets remains challenging.\n\nFINDINGSWe describe the Multigenomic Entropy Based Score pipeline (MEBS), a software platform designed to evaluate, compare and infer complex metabolic pathways in large omic datasets, including entire biogeochemical cycles. MEBS is open source and available through https://github.com/eead-csic-compbio/metagenome_Pfam_score. To demonstrate its use we modeled the sulfur cycle by exhaustively curating the molecular and ecological elements involved (compounds, genes, metabolic pathways and microbial taxa). This information was reduced to a collection of 112 characteristic Pfam protein domains and a list of complete-sequenced sulfur genomes. Using the mathematical framework of relative entropy (H), we quantitatively measured the enrichment of these domains among sulfur genomes. The entropy of each domain was used to both: build up a final score that indicates whether a (meta)genomic sample contains the metabolic machinery of interest and to propose marker domains in metagenomic sequences such as DsrC (PF04358). MEBS was benchmarked with a dataset of 2,107 non-redundant microbial genomes from RefSeq and 935 metagenomes from MG-RAST. Its performance, reproducibility, and robustness were evaluated using several approaches, including random sampling, linear regression models, Receiver Operator Characteristic plots and the Area Under the Curve metric (AUC). Our results support the broad applicability of this algorithm to accurately classify (AUC=0.985) hard to culture genomes (e.g., Candidatus Desulforudis audaxviator), previously characterized ones and metagenomic environments such as hydrothermal vents, or deep-sea sediment.\n\nCONCLUSIONSOur benchmark indicates that an entropy-based score can capture the metabolic machinery of interest and be used to efficiently classify large genomic and metagenomic datasets, including uncultivated/unexplored taxa

bioinformatics↗

A new multi-genomic approach for the study of biogeochemical cycles at global scale: the molecular reconstruction of the sulfur cycle

Despite the great advances in microbial ecology and the explosion of high throughput sequencing, our ability to understand and integrate the global biogeochemical cycles is still limited. Here we propose a novel approach to summarize the complexity of the Sulfur cycle based on the minimum ecosystem concept, the microbial mat model and the relative entropy of protein domains involved in S-metabolism. This methodology produces a single value, called the Sulfur Score (SS), which informs about the specific S-related molecular machinery. After curating an inventory of microorganisms, pathways and genes taking part in this cycle, we benchmark the performance of the SS on a collection of 2,107 non-redundant RefSeq genomes, 900 metagenomes from MG-RAST and 35 metagenomes analyzed for the first time. We find that the SS is able to correctly classify microorganisms known to be involved in the S-cycle, yielding an Area Under the ROC Curve of 0.985. Moreover, when sorting environments the top-scoring metagenomes were hydrothermal vents, microbial mats and deep-sea sediments, among others. This methodology can be generalized to the analysis of other biogeochemical cycles or processes. Provided that an inventory of relevant pathways and microorganisms can be compiled, entropy-based scores could be used to detect environmental patterns and informative samples in multi-genomic scale.

bioinformatics↗