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The \"Latescibacteria\" (formerly WS3), member of the Fibrobacteres-Chlorobi-Bacteroidetes (FCB) superphylum, represents a ubiquitous candidate phylum found in terrestrial, aquatic, and marine ecosystems. Recently, single-cell amplified genomes (SAGs) representing the \"Latescibacteria\" were obtained from the anoxic monimolimnion layers of Sakinaw Lake (British Columbia, Canada), and anoxic sediments of a coastal lagoon (Etoliko lagoon, Western Greece). Here, we present a detailed in-silico analysis of the four SAGs to gain some insights on their metabolic potential and apparent ecological roles. Metabolic reconstruction suggests an anaerobic fermentative mode of metabolism, as well as the capability to degrade multiple polysaccharides and glycoproteins that represent integral components of green (Charophyta and Chlorophyta) and brown (Phaeophycaea) algae cell walls (pectin, alginate, ulvan, fucan, hydroxyproline-rich glycoproteins), storage molecules (starch and trehalose), and extracellular polymeric substances (EPSs). The analyzed SAGs also encode dedicated transporters for the uptake of produced sugars and amino acids/oligopeptides, as well as an extensive machinery for the catabolism of all transported sugars, including the production of a bacterial microcompartment (BMC) to sequester propionaldehyde, a toxic intermediate produced during fucose and rhamnose metabolism. Finally, genes for the formation of gas vesicles, flagella, type IV pili, and oxidative stress response were found, features that could aid in cellular association with algal detritus. Collectively, these results indicate that the analyzed \"Latescibacteria\" mediate the turnover of multiple complex organic polymers of algal origin that reach deeper anoxic/microoxic habitats in lakes and lagoons. The implications of such process on our understanding of niche specialization in microbial communities mediating organic carbon turnover in stratified water bodies are discussed.

We investigated the global patterns of abundance, diversity, and community structure of members of the Aminicenantes (candidate phylum OP8). Our aim was to identify the putative ecological role(s) played by members of this poorly characterized bacterial lineages in various ecosystems. Analysis of near full-length 16S rRNA genes identified four classes and eight orders within the Aminicenantes. Within 3,134 datasets comprising ∼1.8 billion high throughput-generated partial 16S rRNA genes, 47,351 Aminicenantes-affiliated sequences were identified in 913 datasets. The Aminicenantes exhibited the highest relative abundance in hydrocarbon-impacted environments, followed by marine habitats (especially hydrothermal vents and coral-associated microbiome samples), and aquatic, non-marine habitats (especially in terrestrial springs and groundwater samples). While the overall abundance of the Aminicenantes was higher in low oxygen tension as well as non-saline and low salinity habitats, it was encountered in a wide range of oxygen tension, salinities, and temperatures. Analysis of the community structure of the Aminicenantes showed distinct patterns across various datasets that appear to be, mostly, driven by habitat variations rather than prevalent environmental parameters. We argue that the detection of the Aminicenantes across environmental extremes and the observed distinct community structure patterns reflect a high level of intraphylum metabolic diversity and adaptive capabilities that enable its survival and growth in a wide range of habitats and environmental conditions.

Many freshwater lakes undergo seasonal stratification, where the formation of phototrophic blooms in the epilimnion and subsequent sedimentation induces hypoxia/anoxia in the thermocline and hypolimnion. This autochthonously produced biomass represents a major seasonal organic input that impacts the entire ecosystem. While the limnological aspects of this process are fairly well documented, relatively little is known regarding the microbial community response to such events, especially in the deeper anoxic layers of the water column. Here, we conducted a spatiotemporal survey of the particle-associated and free-living microbial communities in a warm monomictic freshwater reservoir (Grand Lake O' the Cherokees) in northeastern Oklahoma, USA. Pre-stratification samples (March) harbored a homogeneous community throughout the oxygenated water column dominated by typical oligotrophic aquatic lineages (acl clade within Actinobacteria, and Flavobacterium within the Bacteroidetes). The onset of phototrophic blooming in June induced the progression of this baseline community into two distinct trajectories. Within the oxic epilimnion, samples were characterized by the propagation of phototrophic (Prochlorococcus), and heterotrophic (Planctomycetes, Verrucomicrobia, and Beta-Proteobacteria) lineages. Within the oxygen-deficient thermocline and hypolimnion, the sedimentation of surface biomass induced the development of a highly diverse community, with the enrichment of Chloroflexi, \"Latescibacteria\", Armatimonadetes, and Delta-Proteobacteria in the particle-associated fraction, and Gemmatimonadetes and \"Omnitrophica\" in the free-living fraction. Our work documents the development of multiple spatially and temporally distinct niches during lake stratification, and supports the enrichment of multiple yet-uncultured and poorly characterized lineages in the lake's deeper oxygen-deficient layers, an ecologically relevant microbial niche that is often overlooked in lakes diversity surveys.

Anaerobic gut fungi (AGF, Neocallimastigomycota ) reside in the alimentary tract of herbivores. While their presence in mammals is well documented, evidence for their occurrence in non-mammalian hosts is currently sparse. Culture-independent surveys of AGF in tortoises identified a unique community, with three novel deep-branching genera representing >90% of sequences in most samples. Representatives of all genera were successfully isolated under strict anaerobic conditions. Transcriptomics-enabled phylogenomic and molecular dating analyses indicated an ancient, deep-branching position in the AGF tree for these genera, with an evolutionary divergence time estimate of 104-112 million years ago (Mya). Such estimates push the establishment of animal- Neocallimastigomycota symbiosis from the late to the early Cretaceous. Further, tortoise-associated isolates (T-AGF) exhibited limited capacity for plant polysaccharides metabolism and lacked genes encoding several carbohydrate-active enzyme (CAZyme) families. Finally, we demonstrate that the observed curtailed degradation capacities and reduced CAZyme repertoire is driven by the paucity of horizontal gene transfer (HGT) in T-AGF genomes, compared to their mammalian counterparts. This reduced capacity was reflected in an altered cellulosomal production capacity in T-AGF. Our findings provide insights into the phylogenetic diversity, ecological distribution, evolutionary history, evolution of fungal-host nutritional symbiosis, and dynamics of genes acquisition in Neocallimastigomycota . Here, Pratt et al identify a community of deep-branching anaerobic fungi in tortoise feces. Multiple characteristics underpinning their success in tortoise, as opposed to scarcity in mammalian alimentary tracts, are presented.

The anaerobic fungus Orpinomyces strain C1A is capable of growth on various types of lignocellulosic substrates, and harbors an impressive reservoir of carbohydrate active enzymes (CAZymes). Using a minimum enzyme cocktail strategy, we constituted a four-component lignocellulolytic cocktail derived from highly transcribed C1A, and evaluated its efficacy against pretreated corn stover and switchgrass. Hydrolysis yields ranged between 65–77.4%, depending on the lignocellulosic substrate and pretreatment applied. Addition of a highly expressed anaerobic fungal swollenin improved hydrolysis yields by up to 7%. Compared to the commercial cocktail CTec2, these anaerobic fungal cocktails provided comparable or slightly lower hydrolysis yields. Further, the differences in efficacy between commercial and anaerobic cocktails were often only realized after extended (168 hr) incubations. Under certain conditions, the hydrolysis yields of the anaerobic fungal cocktail was slightly superior to that realized by CTec2. We attribute the observed high hydrolysis yields to the high specific activity and affinity of the individual enzymes of the cocktail, as well as the high level of synergy and multi-functionality observed in multiple components. Collectively, this effort provides a novel platform for constructing highly effective enzymes for biofuel production and represents the first lignocellulolytic enzyme cocktail created from anaerobic fungal enzymes.

Life on earth evolved in an anoxic setting; however, the identity and fate of microorganisms that thrived in a preoxygenated earth are poorly understood. In Zodletone spring, the prevailing geochemical conditions are remarkably similar to conditions prevailing in surficial earth prior to oxygen buildup in the atmosphere. Life emerged and diversified in the absence of molecular oxygen. The prevailing anoxia and unique sulfur chemistry in the Paleo-, Meso-, and Neoarchean and early Proterozoic eras may have supported microbial communities that differ from those currently thriving on the earth’s surface. Zodletone spring in southwestern Oklahoma represents a unique habitat where spatial sampling could substitute for geological eras namely, from the anoxic, surficial light-exposed sediments simulating a preoxygenated earth to overlaid water column where air exposure simulates oxygen intrusion during the Neoproterozoic era. We document a remarkably diverse microbial community in the anoxic spring sediments, with 340/516 (65.89%) of genomes recovered in a metagenomic survey belonging to 200 bacterial and archaeal families that were either previously undescribed or that exhibit an extremely rare distribution on the current earth. Such diversity is underpinned by the widespread occurrence of sulfite, thiosulfate, tetrathionate, and sulfur reduction and the paucity of sulfate reduction machineries in these taxa. Hence, these processes greatly expand lineages mediating reductive sulfur-cycling processes in the tree of life. An analysis of the overlaying oxygenated water community demonstrated the development of a significantly less diverse community dominated by well-characterized lineages and a prevalence of oxidative sulfur-cycling processes. Such a transition from ancient novelty to modern commonality underscores the profound impact of the great oxygenation event on the earth’s surficial anoxic community. It also suggests that novel and rare lineages encountered in current anaerobic habitats could represent taxa that once thrived in an anoxic earth but have failed to adapt to earth’s progressive oxygenation. IMPORTANCE Life on earth evolved in an anoxic setting; however, the identity and fate of microorganisms that thrived in a preoxygenated earth are poorly understood. In Zodletone spring, the prevailing geochemical conditions are remarkably similar to conditions prevailing in surficial earth prior to oxygen buildup in the atmosphere. We identify hundreds of previously unknown microbial lineages in the spring and demonstrate that these lineages possess the metabolic machinery to mediate a wide range of reductive sulfur processes, with the capacity to respire sulfite, thiosulfate, sulfur, and tetrathionate, rather than sulfate, which is a reflection of the differences in sulfur-cycling chemistry in ancient versus modern times. Collectively, such patterns strongly suggest that microbial diversity and sulfur-cycling processes in a preoxygenated earth were drastically different from the currently observed patterns and that the Great Oxygenation Event has precipitated the near extinction of a wide range of oxygen-sensitive lineages and significantly altered the microbial reductive sulfur-cycling community on earth.

The phylogenetic diversity and community structure of members of the gut anaerobic fungi (AF) (phylum Neocallimastigomycota ) were investigated in 30 different herbivore species that belong to 10 different mammalian and reptilian families using the internal transcribed spacer region-1 (ITS-1) ribosomal RNA (rRNA) region as a phylogenetic marker. A total of 267 287 sequences representing all known anaerobic fungal genera were obtained in this study. Sequences affiliated with the genus Piromyces were the most abundant, being encountered in 28 different samples, and representing 36% of the sequences obtained. On the other hand, sequences affiliated with the genera Cyllamyces and Orpinomyces were the least abundant, being encountered in 2, and 8 samples, and representing 0.7%, and 1.1% of the total sequences obtained, respectively. Further, 38.3% of the sequences obtained did not cluster with previously identified genera and formed eight phylogenetically distinct novel anaerobic fungal lineages. Some of these novel lineages were widely distributed (for example NG1 and NG3), whereas others were animal specific, being encountered in only one or two animals (for example NG4, NG6, NG7, and NG8). The impact of various physiological and environmental factors on the diversity and community structure of AF was examined. The results suggest that animal host phylogeny exerts the most significant role on shaping anaerobic fungal diversity and community composition. These results greatly expand the documented global phylogenetic diversity of members of this poorly studied group of fungi that has an important function in initiating plant fiber degradation during fermentative digestion in ruminant and non-ruminant herbivores.

Focal adhesions (FAs) are large eukaryotic multiprotein complexes that are present in all metazoan cells and function as stable sites of tight adhesion between the extracellular matrix (ECM) and the cell's cytoskeleton. FAs consist of anchor membrane protein (integrins), scaffolding proteins (e.g. α-actinin, talin, paxillin, and vinculin), signaling proteins of the IPP complex (e.g. integrin-linked kinase, α-parvin, and PINCH), and signaling kinases (e.g. focal adhesion kinase (FAK) and Src kinase). While genes encoding complete focal adhesion machineries are present in genomes of all multicellular Metazoa; incomplete machineries were identified in the genomes of multiple non-metazoan unicellular Holozoa, basal fungal lineages, and amoebozoan representatives. Since a complete FA machinery is required for functioning, the putative role, if any, of these incomplete FA machineries is currently unclear. We sought to examine the expression patterns of FA-associated genes in the anaerobic basal fungal isolate Orpinomyces sp. strain C1A under different growth conditions and at different developmental stages. Strain C1A lacks clear homologues of integrin, and the two signaling kinases FAK and Src, but encodes for all scaffolding proteins, and the IPP complex proteins. We developed a protocol for synchronizing growth of C1A cultures, allowing for the collection and mRNA extraction from flagellated spores, encysted germinating spores, active zoosporangia, and late inactive sporangia of strain C1A. We demonstrate that the genes encoding the FA scaffolding proteins α-actinin, talin, paxillin, and vinculin are indeed transcribed under all growth conditions, and at all developmental stages of growth. Further, analysis of the observed transcriptional patterns suggests the putative involvement of these components in alternative non-adhesion-specific functions, such as hyphal tip growth during germination and flagellar assembly during zoosporogenesis. Based on these results, we propose putative alternative functions for such proteins in the anaerobic gut fungi. Our results highlight the presumed diverse functionalities of FA scaffolding proteins in basal fungi.

The AGF are integral part of the microbiome of herbivores. They play a crucial role in breaking down plant biomass in hindgut and foregut fermenters. The majority of research has been conducted on the AGF community in placental mammalian hosts. However, it is important to note that many marsupial mammals are also herbivores and employ a hindgut or foregut fermentation strategy for breaking down plant biomass. So far, very little is known regarding the AGF diversity and community structure in marsupial mammals. To fill this knowledge gap, we conducted an amplicon-based diversity survey targeting AGF in 61 fecal samples from 10 marsupial species. We hypothesize that, given the distinct evolutionary history and alimentary tract architecture, novel and unique AGF communities would be encountered in marsupials. Our results indicate that marsupial AGF communities are highly stochastic, present in relatively low loads, and display community structure patterns comparable to AGF communities typically encountered in placental foregut hosts. Our results indicate that marsupial hosts harbor AGF communities; however, in contrast to the strong pattern of phylosymbiosis typically observed between AGF and placental herbivores, the identity and gut architecture appear to play a minor role in structuring AGF communities in marsupials.

A wide range of microbial lineages remain uncultured, yet little is known regarding their metabolic capacities, physiological preferences, and ecological roles in various ecosystems. We conducted a thorough comparative genomic analysis of 108 genomes belonging to the Binatota (UBP10), a globally distributed, yet-uncharacterized bacterial phylum. The recent leveraging of genome-resolved metagenomics has generated an enormous number of genomes from novel uncultured microbial lineages yet left many clades undescribed. Here, we present a global analysis of genomes belonging to Binatota (UBP10), a globally distributed, yet-uncharacterized bacterial phylum. All orders in Binatota encoded the capacity for aerobic methylotrophy using methanol, methylamine, sulfomethanes, and chloromethanes as the substrates. Methylotrophy in Binatota was characterized by order-specific substrate degradation preferences, as well as extensive metabolic versatility, i.e., the utilization of diverse sets of genes, pathways, and combinations to achieve a specific metabolic goal. The genomes also encoded multiple alkane hydroxylases and monooxygenases, potentially enabling growth on a wide range of alkanes and fatty acids. Pigmentation is inferred from a complete pathway for carotenoids (lycopene, β- and γ-carotenes, xanthins, chlorobactenes, and spheroidenes) production. Further, the majority of genes involved in bacteriochlorophyll a , c , and d biosynthesis were identified, although absence of key genes and failure to identify a photosynthetic reaction center preclude proposing phototrophic capacities. Analysis of 16S rRNA databases showed the preferences of Binatota to terrestrial and freshwater ecosystems, hydrocarbon-rich habitats, and sponges, supporting their potential role in mitigating methanol and methane emissions, breakdown of alkanes, and their association with sponges. Our results expand the lists of methylotrophic, aerobic alkane-degrading, and pigment-producing lineages. We also highlight the consistent encountering of incomplete biosynthetic pathways in microbial genomes, a phenomenon necessitating careful assessment when assigning putative functions based on a set-threshold of pathway completion. IMPORTANCE A wide range of microbial lineages remain uncultured, yet little is known regarding their metabolic capacities, physiological preferences, and ecological roles in various ecosystems. We conducted a thorough comparative genomic analysis of 108 genomes belonging to the Binatota (UBP10), a globally distributed, yet-uncharacterized bacterial phylum. We present evidence that members of the order Binatota specialize in methylotrophy and identify an extensive repertoire of genes and pathways mediating the oxidation of multiple one-carbon (C 1 ) compounds in Binatota genomes. The occurrence of multiple alkane hydroxylases and monooxygenases in these genomes was also identified, potentially enabling growth on a wide range of alkanes and fatty acids. Pigmentation is inferred from a complete pathway for carotenoids production. We also report on the presence of incomplete chlorophyll biosynthetic pathways in all genomes and propose several evolutionary-grounded scenarios that could explain such a pattern. Assessment of the ecological distribution patterns of the Binatota indicates preference of its members to terrestrial and freshwater ecosystems characterized by high methane and methanol emissions, as well as multiple hydrocarbon-rich habitats and marine sponges.