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Saw, J. H.

Publications and source records attributed to Saw, J. H..

8 recordsLinked to original sources

Genome-resolved metagenomics reveals metabolically versatile Actinobacteria with extensive biosynthetic capacity in Hawaiian steam vents

Geothermally active lava caves and hydrothermal steam vents are chemically heterogeneous subsurface environments that harbor diverse microbial communities, yet the ecological and metabolic roles of Actinobacteria in these systems remain poorly characterized. Here, we reconstructed and analyzed 58 actinobacterial metagenome-assembled genomes (MAGs) representing five classes. Comparative genomic analyses revealed broad metabolic versatility, including pathways for amino acid biosynthesis and utilization, central carbon metabolism, fatty acid degradation, and potential chemolithotrophic processes involving carbon monoxide and sulfur compounds. The MAGs also encoded diverse carbohydrate-active enzymes and peptidases suggesting substantial capacity for complex organic carbon and protein utilization. Genome mining identified 219 biosynthetic gene clusters spanning terpenes, ribosomally synthesized and post-translationally modified peptides, nonribosomal peptide synthetases, polyketide synthases, and {beta}-lactones, highlighting extensive secondary-metabolite biosynthetic potential. Antibiotic resistance-associated genes were also detected in several MAGs, with glycopeptide-resistance-associated van genes particularly prevalent among Thermoleophilia. Sequence similarity network analysis revealed that several van-associated proteins from Thermoleophilia and UBA4738 shared substantial sequence similarity with homologs from other environmental Actinobacteria, suggesting broad conservation of these protein families. Collectively, these findings reveal metabolically and functionally diverse Actinobacteria with the genomic potential to participate in carbon and nutrient cycling, microbial interactions, secondary metabolism, and antibiotic resistance in geothermally active ecosystems.

microbiology↗

Hawaiian Geothermal Fumaroles Contain Diverse and Novel Viruses

Microbial communities of geothermal habitats are central to understanding the evolution of life on Earth. Metagenomics has provided insight into the role of viruses in shaping microbial diversity of complex environments. However, identification of novel viruses is constrained by lack of marker genes and low nucleotide similarities between related viral taxa. While microbial and viral diversity have been explored in terrestrial hot springs and hydrothermal vent systems, other volcanic features remain underexplored. Fumaroles (steam vents) are geothermal features that heat groundwater with magma, releasing steam and volcanic gases such as CO2 and H2S. Comparatively physicochemically dynamic to hot springs, fumarole temperatures and gas emissions rapidly fluctuate with volcanic activity. Here, we describe viruses identified metagenomically from microbial mats hosted near basaltic fumaroles on the Big Island of Hawaii. To our knowledge, this is the first systematic survey of fumarole viruses. Our utilization of a sensitive profile-based approach for identification reveals high viral diversity in fumaroles, resulting in estimation of two undescribed order-level clades of Caudoviricetes (tailed phages). Viral metabolic genes provide evidence of viral-mediated adaptation of microbes to fumarole conditions. We describe patterns of viral diversity that diverge from the Bank model of viral ecology, hinting at viral dispersal between biofilms and high viral richness and evenness. Lastly, we provide a description of the first terrestrial geothermal environment dominated by Microviridae, previously only described in viral communities of deep ocean hydrothermal vents. This study offers important findings for exploration of viral ecology in extreme environments.

microbiology↗

Amplicon and metagenomic data from fumarole-associated geothermal features of Hawaii

The Hawaiian islands are among the most geologically and volcanically active places on Earth. While the Hawaiian Archipelago is known for its animal and plant diversity, much less is known about microbial diversity in the areas diverse habitats. In this study, we focused on steam vent associated biofilms found on the most volcanically active island of Hawai{square}i, also known as the Big Island. From 46 samples from various biofilms and associated features around fumaroles emitting water steam, we generated amplicon and metagenomic sequences. Amplicon data showed that Chloroflexota and Cyanobacteriota are the numerically dominant phyla in these biofilm communities. We constructed 363 non-redundant medium to high-quality metagenome-assembled genomes (MAGs) that are at least 70% complete and with less than 5% contamination. Ten MAGs belong in the domain Archaea, and 353 belong in the domain Bacteria. This dataset could provide valuable insights into microbial diversity and ecology around volcanic features in Hawai i and elsewhere.

microbiology↗

Taxonomic Description of Uncultured Cyanobacteria from Extreme Habitats through Genome-Based Classification

Cyanobacteria form a morphologically and phylogenetically diverse group of oxygenic phototrophic bacteria inhabiting a wide range of environments, including extreme habitats such as hot springs and volcanic steam vents. Many lineages, particularly those from these extreme environments, remain uncultured and are known only from metagenome-assembled genomes (MAGs), limiting their integration into formal taxonomy. Analysis of 46 steam vent associated samples from Hawai i using 16S rRNA amplicon sequencing revealed that cyanobacteria dominate these communities. Gloeobacter kilaueensis dominated pit-like environments with low-light conditions, while Leptolyngbyaceae and other families are more dominant in structured soil and wall communities. We further reconstructed 38 high-quality cyanobacterial MAGs and incorporated them into a phylogenomic analysis comprising 343 cyanobacterial genomes, followed by genome-based comparisons against 9,026 reference genomes. This revealed eight novel species and one novel genus spanning five orders: Chroococcidiopsidales, Leptolyngbyales, Nostocales, Oculatellales, and Oscillatoriales. Following SeqCode guidelines, we provide the first formal taxonomic descriptions of cyanobacterial MAGs and propose guidelines for integrating genome-based and cultivated material. These findings highlight Hawaiian steam vents as hotspots of previously uncharacterized cyanobacterial diversity and underscore the importance of genome-based nomenclature.

genomics↗

Early-Diverging SQR Enzyme in Antarctic Gloeobacterales Indicates Sulfide Tolerance in Thylakoid-Lacking Cyanobacteria

Oxygenic photosynthesis, which converts solar energy into carbohydrates via a linear electron transport chain and two photosystems (PSII and PSI), first appeared in cyanobacteria approximately 3.3 Ga and drove the Great Oxidation Event around 2.4 Ga. During this period, euxinic conditions--characterized by sulfidic, anoxic oceans--posed a metabolic challenge to cyanobacteria, as sulfide inhibits PSII, the reaction center responsible for water splitting. Here, we report the presence of an early-diverging form of the sulfide quinone reductase (SQR) enzyme in Antarctic representatives of Gloeobacterales, the earliest-branching cyanobacterial lineage lacking thylakoids. Phylogenetic analyses reveal that these SQR sequences are the earliest-diverging cyanobacterial SQR known to date, predating the multiple lateral gene transfer events previously observed in the phylum. Additional searches in metagenomic datasets indicate that such sequences are restricted to cold environments. Our findings unveil possible adaptive strategies of early cyanobacteria to cope with sulfidic stress and point to Antarctic lakes as preserved natural laboratories for investigating cyanobacterial diversification and the evolution of oxygenic photosynthesis under euxinic conditions. Impact StatementThe diversification of cyanobacteria during and after the Great Oxidation Event occurred in early Proterozoic oceans that were partially euxinic (anoxic and sulfidic) a condition generally considered incompatible with oxygenic photosynthesis due to photosystem II inhibition. The presence of a sulfide quinone reductase in an Antarctic early diverging cyanobacterium lacking thylakoids gives credit on an ancestral evolutionary stage where oxygenic and anoxygenic traits coexisted within cyanobacteria. The occurrence of these organisms in Antarctic lakes under euxinic conditions offers a natural laboratory for studying the physiology and adaptation of the first oxygenic photosynthetic organisms.

evolutionary biology↗

Phylogenomics and ancestral reconstruction of Korarchaeota reveals genomic adaptation to habitat switching

Our knowledge of archaeal diversity and evolution has expanded rapidly in the past decade. However, hardly any genomes of the phylum Korarchaeota have been obtained due to the difficulty in accessing their natural habitats and - possibly - their limited abundance. As a result, many aspects of Korarchaeota biology, physiology and evolution remain enigmatic. Here, we expand this phylum with five high-quality metagenome-assembled genomes. This improved taxon sampling combined with sophisticated phylogenomic analyses robustly places Korarchaeota at the base of TACK and Asgard clades, revisiting the phylums long-assumed position. Furthermore, we observe a clear split between terrestrial and marine thermal clades. Gene tree-aware ancestral reconstructions suggest that the last Korarchaeota common ancestor was a thermophilic autotroph. In contrast, Korarchaeaceae, the lineage where environmental transitions occurred, shifted towards a heterotrophic lifestyle. Terrestrial Korarchaeota gained many cas and CARF genes indicating they may need to manage viral infections. Together, our study provides new insights into these early diverging Archaea and suggests that gradual gene gain and loss shaped their adaptation to different thermal environments. ImportanceKorarchaeota are an ancient group of archaea, but their biology, physiology and evolution have remained obscure. Analysis of five novel Korarchaeota MAGs, and publicly available reference data provides robust phylogenomic evidence that Korarchaeota are placed at the base of Asgard archaea and TACK, revisiting the phylums long-assumed position. Gene content reconstruction suggests a versatile thermophilic and autotrophic last Korarchaeota common ancestor. Environmental distribution surveying of public databases places all Korarchaeota in thermophilic environments and indicates that their habitat is limited to hydrothermal vents and hot springs. Our modeling indicates at least two transitions linked to habitat switching between these environments in the evolutionary history of Korarchaeota. Both are linked to a significant alteration of the inferred ancestral gene content, including a shift towards a heterotrophic and potential scavenging lifestyle. Furthermore, hot spring Korarchaeota acquired various genes participating in resistance to viruses, suggesting they may need to manage frequent viral threats.

microbiology↗

Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes

In the ongoing debates about eukaryogenesis, the series of evolutionary events leading to the emergence of the eukaryotic cell from prokaryotic ancestors, members of the Asgard archaea play a key role as the closest archaeal relatives of eukaryotes. However, the nature and phylogenetic identity of the last common ancestor of Asgard archaea and eukaryotes remain unresolved. Here, we analyze distinct phylogenetic marker datasets of an expanded genomic sampling of Asgard archaea and evaluate competing evolutionary scenarios using state-of-the-art phylogenomic approaches. We find that eukaryotes are placed, with high confidence, as a well-nested clade within Asgard archaea, as a sister lineage to Hodarchaeales, a newly proposed order within Heimdallarchaeia. Using sophisticated gene tree/species tree reconciliation approaches, we show that, in analogy to the evolution of eukaryotic genomes, genome evolution in Asgard archaea involved significantly more gene duplication and fewer gene loss events compared to other archaea. Finally, we infer that the last common ancestor of Asgard archaea likely was a thermophilic chemolithotroph, and that the lineage from which eukaryotes evolved adapted to mesophilic conditions and acquired the genetic potential to support a heterotrophic lifestyle. Our work provides key insights into the prokaryote-to-eukaryote transition and the platform for the emergence of cellular complexity in eukaryotic cells.

evolutionary biology↗

Pangenomics reveal diversification of enzyme families and niche specialization in globally abundant SAR202 bacteria

It has been hypothesized that abundant heterotrophic ocean bacterioplankton in the SAR202 clade of the phylum Chloroflexi evolved specialized metabolism for the oxidation of organic compounds that are resistant to microbial degradation via common metabolic pathways. Expansions of paralogous enzymes were reported and implicated in hypothetical metabolism involving monooxygenase and dioxygenase enzymes. In the metabolic schemes proposed, the paralogs serve the purpose of diversifying the range of organic molecules that cells can utilize. To further explore this question, we reconstructed SAR202 single amplified genomes and metagenome-assembled genomes from locations around the world, including the deepest ocean trenches. In analyses of 122 SAR202 genomes that included six subclades spanning SAR202 diversity, we observed additional evidence of paralog expansions that correlated with evolutionary history, and further evidence of metabolic specialization. Consistent with previous reports, families of flavin-dependent monooxygenases were observed mainly in the Group III SAR202, in the proposed class Monstramaria and expansions of dioxygenase enzymes were prevalent in Group IV. We found that Group I SAR202 encode expansions of racemases in the enolase superfamily, which we propose evolved for the degradation of compounds that resist biological oxidation because of chiral complexity. Supporting the conclusion that the paralog expansions indicate metabolic specialization, fragment recruitment and fluorescence in situ hybridization with phylogenetic probes showed that SAR202 subclades are indigenous to different ocean depths and geographical regions. Surprisingly, some of the subclades were abundant in surface waters and contained rhodopsin genes, altering our understanding of the ecological role of SAR202 in stratified water columns.\n\nImportanceThe oceans contain an estimated 662 Pg C of dissolved organic carbon (DOC). Information about microbial interactions with this vast resource is limited, despite broad recognition that DOM turnover has a major impact on the global carbon cycle. To explain patterns in the genomes of marine bacteria we propose hypothetical metabolic pathways for the oxidation of organic molecules that are resistant to oxidation via common pathways. The hypothetical schemes we propose suggest new metabolism and classes of compounds that could be important for understanding of the distribution of organic carbon throughout the biosphere. These genome-based schemes will remain hypothetical until evidence from experimental cell biology can be gathered to test them, but until then they provide a perspective that directs our attention to the biochemistry of resistant DOM metabolism. Our findings also fundamentally change our understanding of the ecology of SAR202, showing that metabolically diverse variants of these cells occupy niches spanning all depths, and are not relegated to the dark ocean.

genomics↗