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Woyke, T.

Publications and source records attributed to Woyke, T..

5 recordsLinked to original sources

Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens

Methanogenic archaea are major contributors to the global carbon cycle and were long thought to belong exclusively to the euryarchaeotal phylum. Discovery of the methanogenesis gene cluster methyl-coenzyme M reductase (Mcr) in the Bathyarchaeota and thereafter the Verstraetearchaeota led to a paradigm shift, pushing back the evolutionary origin of methanogenesis to pre-date that of the Euryarchaeota. The methylotrophic methanogenesis found in the non-Euryarchaota distinguished itself from the predominantly hydrogenotrophic methanogens found in euryarchaeal orders as the former do not couple methanogenesis to carbon fixation through the reductive acetyl-coenzyme A (Wood-Ljungdahl) pathway, which was interpreted as evidence for independent evolution of the two methanogenesis pathways. Here, we report the discovery of a complete and divergent hydrogenotrophic methanogenesis pathway in a novel, thermophilic order of the Verstraetearchaeota which we have named Candidatus Methanohydrogenales, as well as the presence of the Wood-Ljungdahl pathway in the crenarchaeal order Desulfurococcales. Our findings support the ancient origin of hydrogenotrophic methanogenesis, suggest that methylotrophic methanogenesis might be a later adaptation of specific orders, and provide insight into how transition from hydrogenotrophic to methylotrophic methanogenesis might occur.

microbiology

Hydrogen-based metabolism - An ancestral trait in lineages sibling to the Cyanobacteria

The metabolic machinery from which microbial aerobic respiration evolved is tightly linked to the origins of oxygenic Cyanobacteria (Oxyphotobacteria). Even though the majority of Oxyphotobacteria are photoautotrophs and can use carbohydrates with oxygen (O2) as the electron acceptor, all are fermenters under dark anoxic conditions. Studies suggest that the ancestor of Oxyphotobacteria may have used hydrogen (H2) as an electron donor and that two types of NiFe hydrogenases are essential for its oxidation. Melainabacteria and Sericytochromatia, close phylogenetic neighbors to Oxyphotobacteria comprise fermentative and aerobic representatives, or organisms capable of both. Margulisbacteria (candidate divisions RBX-1 and ZB3) and Saganbacteria (candidate division WOR-1), a novel cluster of bacteria phylogenetically related to Melainabacteria, Sericytochromatia and Oxyphotobacteria may further constrain the metabolic platform in which oxygenic photosynthesis and aerobic respiration arose. Here, we predict the metabolisms of Margulisbacteria and Saganbacteria from new and published metagenome-assembled genomes (MAGs) and single amplified genomes (SAGs), and compare them to their phylogenetic neighbors. Sediment-associated Margulisbacteria are predicted to have a fermentation-based metabolism featuring a variety of hydrogenases, a nitrogenase for nitrogen (N2) fixation, and electron bifurcating complexes involved in cycling of ferredoxin and NAD(P)H. Overall, the genomic features suggest the capacity for metabolic fine-tuning under strictly anoxic conditions. In contrast, the genomes of Margulisbacteria from the ocean ecosystem encode an electron transport chain that supports aerobic growth. Similarly, some Saganbacteria genomes encode various hydrogenases, and others may have the ability to use O2 under certain conditions via a putative novel type of heme copper O2 reductase. Like Melainabacteria and Sericytochromatia, Margulisbacteria and Saganbacteria have diverse energy metabolisms capable of fermentation, and aerobic or anaerobic respiration. In summary, our findings support the hypothesis that the ancestor of these groups was an anaerobe in which fermentation and H2 metabolism were central metabolic features. Our genomic data also suggests that contemporary lineages sibling to the Oxyphotobacteria may have acquired the ability to use O2 as a terminal electron acceptor under certain environmental conditions.

microbiology

Archaeal, bacterial, and eukaryal microbial community structure of sediment and seawater in a coastal region near Puerto Nuevo, Baja California

Microbial communities control numerous biogeochemical processes critical for ecosystem function and health, particularly in coastal ecosystems. However, comparatively little is known about microbial community structure in coastal regions, such that basic patterns of microbial biodiversity, such as species richness and community composition, are generally understudied. To better understand the global patterns of microbial biodiversity in coastal ecosystems, we characterized sediment and seawater microbial communities for three sites near Puerto Nuevo (Baja California, Mexico) using 16S and 18S rRNA gene amplicon sequencing methods. We found that sediment bacteria, archaea, and eukaryote microbial communities contained approximately 5 x 10^2 fold greater operational taxonomic units (OTUs) than their seawater-based counterparts (p < 0.001). Further, distinct bacterial, archaeal and eukaryal phyla were found in sediment and seawater samples. The phyla Acidobacteria, Chlorobi, and Chloroflexi were found to be abundant and unique to the sediment and Cyanobacteria, Spirochaetae, and Woesearchaeota to the seawater environment. Apicomplexa and Arthropoda were abundant eukaryal phyla found uniquely in the sediment whereas the Cryptomonadales and Protalveolata were detected only in the seawater. Furthermore, bacterial and archaeal communities were statistically different by site (p < 0.05) in both seawater and sediment samples for the Major Outlet site, the site closest to a residential area. In contrast, eukaryal microbial communities were only different among sites in the seawater samples. Overall, these results suggest that our understanding of coastal microbial biodiversity patterns require spatially robust sampling. This study contributes to a growing body of foundational microbial biodiversity and ecology knowledge, providing context to the global change that is induced by urban development.

microbiology

Solagigasbacteria: Lone genomic giants among the uncultured bacterial phyla

Recent advances in single-cell genomic and metagenomic techniques have facilitated the discovery of numerous previously unknown, deep branches of the tree of life that lack cultured representatives. Many of these candidate phyla are composed of microorganisms with minimalistic, streamlined genomes lacking some core metabolic pathways, which may contribute to their resistance to growth in pure culture. Here we analyzed single-cell genomes and metagenome bins to show that the \"Candidate phylum SPAM\" represents an interesting exception, by having large genomes (6-8 Mbps), high GC content (66%-71%), and the potential for a versatile, mixotrophic metabolism. We also observed an unusually high genomic heterogeneity among individual SPAM cells in the studied samples. These features may have contributed to the limited recovery of sequences of this candidate phylum in prior metagenomic studies. Based on these observations, we propose renaming SPAM to \"Candidate phylum Solagigasbacteria\". Current evidence suggests that Solagigasbacteria are distributed globally in diverse terrestrial ecosystems, including soils, the rhizosphere, volcanic mud, oil wells, aquifers and the deep subsurface, with no reports from marine environments to date.

microbiology

Microfluidic-based mini-metagenomics enables discovery of novel microbial lineages from complex environmental samples

Metagenomics and single-cell genomics have enabled the discovery of many new genomes from previously unknown branches of life. However, extracting novel genomes from complex mixtures of metagenomic data can still be challenging and in many respects represents an ill-posed problem which is generally approached with ad hoc methods. Here we present a microfluidic-based mini-metagenomic method which offers a statistically rigorous approach to extract novel microbial genomes from complex samples. In addition, by generating 96 sub-samples from each environmental sample, this method maintains high throughput, reduces sample complexity, and preserves single-cell resolution. We used this approach to analyze two hot spring samples from Yellowstone National Park and extracted 29 new genomes larger than 0.5 Mbps. These genomes represent novel lineages at different taxonomic levels, including three deeply branching lineages. Functional analysis revealed that these organisms utilize diverse pathways for energy metabolism. The resolution of this mini-metagenomic method enabled accurate quantification of genome abundance, even for genomes less than 1% in relative abundance. Our analyses also revealed a wide range of genome level single nucleotide polymorphism (SNP) distributions with nonsynonymous to synonymous ratio indicative of low to moderate environmental selection. The scale, resolution, and statistical power of microfluidic-based mini-metagenomic make it a powerful tool to dissect the genomic structure microbial communities while effectively preserving the fundamental unit of biology, the single cell.

microbiology