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1. An ecological-evolutionary perspective on the genomic diversity and habitat preferences of the Acidobacteriota

   https://doi.org/10.1099/mgen.0.001344  

   McReynolds, Ella; Elshahed, Mostafa S; Youssef, Noha H (January 2025, Microbial Genomics)

   Members of the phylumAcidobacteriotainhabit a wide range of ecosystems including soils. We analysed the global patterns of distribution and habitat preferences of variousAcidobacteriotalineages across major ecosystems (soil, engineered, host-associated, marine, non-marine saline and alkaline and terrestrial non-soil ecosystems) in 248 559 publicly available metagenomic datasets. ClassesTerriglobia,Vicinamibacteria,BlastocatelliaandThermoanaerobaculiawere highly ubiquitous and showed a clear preference to soil over non-soil habitats, while classesAminicenantiaandHolophagaeshowed preferences to non-soil habitats. However, while specific preferences were observed, mostAcidobacteriotalineages were habitat generalists rather than specialists, with genomic and/or metagenomic fragments recovered from soil and non-soil habitats at various levels of taxonomic resolution. Comparative analysis of 1930 genomes strongly indicates that phylogenetic affiliation plays a more important role than the habitat from which the genome was recovered in shaping the genomic characteristics and metabolic capacities of theAcidobacteriota. The observed lack of strong habitat specialization and habitat-transition-driven lineage evolution in theAcidobacteriotasuggest ready cross-colonization between soil and non-soil habitats. We posit that such capacity is key to the successful establishment ofAcidobacteriotaas a major component in soil microbiomes post-ecosystem disturbance events or during pedogenesis. 

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2. Genomic Variation Influences Methanothermococcus Fitness in Marine Hydrothermal Systems

   https://doi.org/10.3389/fmicb.2021.714920  

   Hoffert, Michael; Anderson, Rika E.; Reveillaud, Julie; Murphy, Leslie G.; Stepanauskas, Ramunas; Huber, Julie A. (August 2021, Frontiers in Microbiology)

   Hydrogenotrophic methanogens are ubiquitous chemoautotrophic archaea inhabiting globally distributed deep-sea hydrothermal vent ecosystems and associated subseafloor niches within the rocky subseafloor, yet little is known about how they adapt and diversify in these habitats. To determine genomic variation and selection pressure within methanogenic populations at vents, we examined five Methanothermococcus single cell amplified genomes (SAGs) in conjunction with 15 metagenomes and 10 metatranscriptomes from venting fluids at two geochemically distinct hydrothermal vent fields on the Mid-Cayman Rise in the Caribbean Sea. We observed that some Methanothermococcus lineages and their transcripts were more abundant than others in individual vent sites, indicating differential fitness among lineages. The relative abundances of lineages represented by SAGs in each of the samples matched phylogenetic relationships based on single-copy universal genes, and genes related to nitrogen fixation and the CRISPR/Cas immune system were among those differentiating the clades. Lineages possessing these genes were less abundant than those missing that genomic region. Overall, patterns in nucleotide variation indicated that the population dynamics of Methanothermococcus were not governed by clonal expansions or selective sweeps, at least in the habitats and sampling times included in this study. Together, our results show that although specific lineages of Methanothermococcus co-exist in these habitats, some outcompete others, and possession of accessory metabolic functions does not necessarily provide a fitness advantage in these habitats in all conditions. This work highlights the power of combining single-cell, metagenomic, and metatranscriptomic datasets to determine how evolution shapes microbial abundance and diversity in hydrothermal vent ecosystems. 

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3. Genomic characterization of three novel Desulfobacterota classes expand the metabolic and phylogenetic diversity of the phylum

   https://doi.org/10.1111/1462-2920.15614  

   Murphy, Chelsea_L; Biggerstaff, James; Eichhorn, Alexis; Ewing, Essences; Shahan, Ryan; Soriano, Diana; Stewart, Sydney; VanMol, Kaitlynn; Walker, Ross; Walters, Payton; et al (June 2021, Environmental Microbiology)

   Summary We report on the genomic characterization of three novel classes in the phylum Desulfobacterota. One class (proposed nameCandidatus‘Anaeroferrophillalia’) was characterized by heterotrophic growth capacity, either fermentatively or utilizing polysulfide, tetrathionate or thiosulfate as electron acceptors. In the absence of organic carbon sources, autotrophic growth via the Wood–Ljungdahl (WL) pathway and using hydrogen or Fe(II) as an electron donor is also inferred for members of the ‘Anaeroferrophillalia’. The second class (proposed nameCandidatus‘Anaeropigmentia’) was characterized by its capacity for growth at low oxygen concentration, and the capacity to synthesize the methyl/alkyl carrier CoM, an ability that is prevalent in the archaeal but rare in the bacterial domain. Pigmentation is inferred from the capacity for carotenoid (lycopene) production. The third class (proposed nameCandidatus‘Zymogenia’) was characterized by fermentative heterotrophic growth capacity, broad substrate range and the adaptation of some of its members to hypersaline habitats. Analysis of the distribution pattern of all three classes showed their occurrence as rare community members in multiple habitats, with preferences for anaerobic terrestrial, freshwater and marine environments over oxygenated (e.g. pelagic ocean and agricultural land) settings. Special preference for some members of the classCandidatus‘Zymogenia’ for hypersaline environments such as hypersaline microbial mats and lagoons was observed. 

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4. Modelling the habitat preference of two key <i>Sphagnum</i> species in a poor fen as controlled by capitulum water content

   https://doi.org/10.5194/bg-17-5693-2020  

   Gong, Jinnan; Roulet, Nigel; Frolking, Steve; Peltola, Heli; Laine, Anna M.; Kokkonen, Nicola; Tuittila, Eeva-Stiina (January 2020, Biogeosciences)

   null (Ed.)

   Abstract. Current peatland models generally treat vegetation as static, although plant community structure is known to alter as a response to environmental change. Because the vegetation structure and ecosystem functioning are tightly linked, realistic projections of peatland response to climate change require the inclusion of vegetation dynamics in ecosystem models. In peatlands, Sphagnum mosses are key engineers. Moss community composition primarily follows habitat moisture conditions. The known species habitat preference along the prevailing moisture gradient might not directly serve as a reliable predictor for future species compositions, as water table fluctuation is likely to increase. Hence, modelling the mechanisms that control the habitat preference of Sphagna is a good first step for modelling community dynamics in peatlands. In this study, we developed the Peatland Moss Simulator (PMS), which simulates the community dynamics of the peatland moss layer. PMS is a process-based model that employs a stochastic, individual-based approach for simulating competition within the peatland moss layer based on species differences in functional traits. At the shoot-level, growth and competition were driven by net photosynthesis, which was regulated by hydrological processes via the capitulum water content. The model was tested by predicting the habitat preferences of Sphagnum magellanicum and Sphagnum fallax – two key species representing dry (hummock) and wet (lawn) habitats in a poor fen peatland (Lakkasuo, Finland). PMS successfully captured the habitat preferences of the two Sphagnum species based on observed variations in trait properties. Our model simulation further showed that the validity of PMS depended on the interspecific differences in the capitulum water content being correctly specified. Neglecting the water content differences led to the failure of PMS to predict the habitat preferences of the species in stochastic simulations. Our work highlights the importance of the capitulum water content with respect to the dynamics and carbon functioning of Sphagnum communities in peatland ecosystems. Thus, studies of peatland responses to changing environmental conditions need to include capitulum water processes as a control on moss community dynamics. Our PMS model could be used as an elemental design for the future development of dynamic vegetation models for peatland ecosystems. 

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5. Genomic Analysis of the Yet-Uncultured Binatota Reveals Broad Methylotrophic, Alkane-Degradation, and Pigment Production Capacities

   https://doi.org/10.1128/mBio.00985-21  

   Murphy, Chelsea L.; Sheremet, Andriy; Dunfield, Peter F.; Spear, John R.; Stepanauskas, Ramunas; Woyke, Tanja; Elshahed, Mostafa S.; Youssef, Noha H. (June 2021, mBio)

   Harwood, Caroline S. (Ed.)

   ABSTRACT 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. 

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