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1. Diversity at single nucleotide to pangenome scales among sulfur cycling bacteria in salt marshes

   https://doi.org/10.1128/aem.00988-23  

   Pérez Castro, Sherlynette ; Peredo, Elena L. ; Mason, Olivia U. ; Vineis, Joseph ; Bowen, Jennifer L. ; Mortazavi, Behzad ; Ganesh, Anakha ; Ruff, S. Emil ; Paul, Blair G. ; Giblin, Anne E. ; et al ( November 2023 , Applied and Environmental Microbiology)

   Glass, Jennifer B. (Ed.)

   Sulfur-cycling microbial communities in salt marsh rhizosphere sediments mediate a recycling and detoxification system central to plant productivity. Despite the importance of sulfur-cycling microbes, their biogeographic, phylogenetic, and functional diversity remain poorly understood. Here, we use metagenomic data sets from Massachusetts (MA) and Alabama (AL) salt marshes to examine the distribution and genomic diversity of sulfur-cycling plant-associated microbes. Samples were collected from sediments underSporobolus alterniflorusandSporobolus pumilusin separate MA vegetation zones, and underS. alterniflorusandJuncus roemerianusco-occuring in AL. We grouped metagenomic data by plant species and site and identified 38 MAGs that included pathways for sulfate reduction or sulfur oxidation. Phylogenetic analyses indicated that 29 of the 38 were affiliated with uncultivated lineages. We showed differentiation in the distribution of MAGs between AL and MA, betweenS. alterniflorusandS. pumilusvegetation zones in MA, but no differentiation betweenS. alterniflorusandJ. roemerianusin AL. Pangenomic analyses of eight ubiquitous MAGs also detected site- and vegetation-specific genomic features, including varied sulfur-cycling operons, carbon fixation pathways, fixed single-nucleotide variants, and active diversity-generating retroelements. This genetic diversity, detected at multiple scales, suggests evolutionary relationships affected by distance and local environment, and demonstrates differential microbial capacities for sulfur and carbon cycling in salt marsh sediments.

   Salt marshes are known for their significant carbon storage capacity, and sulfur cycling is closely linked with the ecosystem-scale carbon cycling in these ecosystems. Sulfate reducers are key for the decomposition of organic matter, and sulfur oxidizers remove toxic sulfide, supporting the productivity of marsh plants. To date, the complexity of coastal environments, heterogeneity of the rhizosphere, high microbial diversity, and uncultured majority hindered our understanding of the genomic diversity of sulfur-cycling microbes in salt marshes. Here, we use comparative genomics to overcome these challenges and provide an in-depth characterization of sulfur-cycling microbial diversity in salt marshes. We characterize communities across distinct sites and plant species and uncover extensive genomic diversity at the taxon level and specific genomic features present in MAGs affiliated with uncultivated sulfur-cycling lineages. Our work provides insights into the partnerships in salt marshes and a roadmap for multiscale analyses of diversity in complex biological systems.

    

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2. Genomic reconstruction of fossil and living microorganisms in ancient Siberian permafrost

   https://doi.org/10.1186/s40168-021-01057-2  

   Liang, Renxing ; Li, Zhou ; Lau Vetter, Maggie C. Y. ; Vishnivetskaya, Tatiana A. ; Zanina, Oksana G. ; Lloyd, Karen G. ; Pfiffner, Susan M. ; Rivkina, Elizaveta M. ; Wang, Wei ; Wiggins, Jessica ; et al ( May 2021 , Microbiome)

   Total DNA (intracellular, iDNA and extracellular, eDNA) from ancient permafrost records the mixed genetic repository of the past and present microbial populations through geological time. Given the exceptional preservation of eDNA under perennial frozen conditions, typical metagenomic sequencing of total DNA precludes the discrimination between fossil and living microorganisms in ancient cryogenic environments. DNA repair protocols were combined with high throughput sequencing (HTS) of separate iDNA and eDNA fraction to reconstruct metagenome-assembled genomes (MAGs) from ancient microbial DNA entrapped in Siberian coastal permafrost.

   Despite the severe DNA damage in ancient permafrost, the coupling of DNA repair and HTS resulted in a total of 52 MAGs from sediments across a chronosequence (26–120 kyr). These MAGs were compared with those derived from the same samples but without utilizing DNA repair protocols. The MAGs from the youngest stratum showed minimal DNA damage and thus likely originated from viable, active microbial species. Many MAGs from the older and deeper sediment appear related to past aerobic microbial populations that had died upon freezing. MAGs from anaerobic lineages, includingAsgardarchaea, however exhibited minimal DNA damage and likely represent extant living microorganisms that have become adapted to the cryogenic and anoxic environments. The integration of aspartic acid racemization modeling and metaproteomics further constrained the metabolic status of the living microbial populations. Collectively, combining DNA repair protocols with HTS unveiled the adaptive strategies of microbes to long-term survivability in ancient permafrost.

   Our results indicated that coupling of DNA repair protocols with simultaneous sequencing of iDNA and eDNA fractions enabled the assembly of MAGs from past and living microorganisms in ancient permafrost. The genomic reconstruction from the past and extant microbial populations expanded our understanding about the microbial successions and biogeochemical alterations from the past paleoenvironment to the present-day frozen state. Furthermore, we provided genomic insights into long-term survival mechanisms of microorganisms under cryogenic conditions through geological time. The combined strategies in this study can be extrapolated to examine other ancient non-permafrost environments and constrain the search for past and extant extraterrestrial life in permafrost and ice deposits on Mars.

    

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3. “ Candidatus Subterrananammoxibiaceae,” a New Anammox Bacterial Family in Globally Distributed Marine and Terrestrial Subsurfaces

   https://doi.org/10.1128/aem.00800-23  

   Zhao, Rui ; Le Moine Bauer, Sven ; Babbin, Andrew R. ( January 2023 , Applied and Environmental Microbiology)

   Spear, John R. (Ed.)

   ABSTRACT Bacteria specialized in anaerobic ammonium oxidation (anammox) are widespread in many anoxic habitats and form an important functional guild in the global nitrogen cycle by consuming bio-available nitrogen for energy rather than biomass production. Due to their slow growth rates, cultivation-independent approaches have been used to decipher their diversity across environments. However, their full diversity has not been well recognized. Here, we report a new family of putative anammox bacteria, “ Candidatus Subterrananammoxibiaceae,” existing in the globally distributed terrestrial and marine subsurface (groundwater and sediments of estuary, deep-sea, and hadal trenches). We recovered a high-quality metagenome-assembled genome of this family, tentatively named “ Candidatus Subterrananammoxibius californiae,” from a California groundwater site. The “ Ca. Subterrananammoxibius californiae” genome not only contains genes for all essential components of anammox metabolism (e.g., hydrazine synthase, hydrazine oxidoreductase, nitrite reductase, and nitrite oxidoreductase) but also has the capacity for urea hydrolysis. In an Arctic ridge sediment core where redox zonation is well resolved, “ Ca. Subterrananammoxibiaceae” is confined within the nitrate-ammonium transition zone where the anammox rate maximum occurs, providing environmental proof of the anammox activity of this new family. Phylogenetic analysis of nitrite oxidoreductase suggests that a horizontal transfer facilitated the spreading of the nitrite oxidation capacity between anammox bacteria (in the Planctomycetota phylum) and nitrite-oxidizing bacteria from Nitrospirota and Nitrospinota . By recognizing this new anammox family, we propose that all lineages within the “ Ca. Brocadiales” order have anammox capacity. IMPORTANCE Microorganisms called anammox bacteria are efficient in removing bioavailable nitrogen from many natural and human-made environments. They exist in almost every anoxic habitat where both ammonium and nitrate/nitrite are present. However, only a few anammox bacteria have been cultured in laboratory settings, and their full phylogenetic diversity has not been recognized. Here, we present a new bacterial family whose members are present across both the terrestrial and marine subsurface. By reconstructing a high-quality genome from the groundwater environment, we demonstrate that this family has all critical enzymes of anammox metabolism and, notably, also urea utilization. This bacterium family in marine sediments is also preferably present in the niche where the anammox process occurs. These findings suggest that this novel family, named “ Candidatus Subterrananammoxibiaceae,” is an overlooked group of anammox bacteria, which should have impacts on nitrogen cycling in a range of environments. 

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4. Variation in gut microbial contribution of essential amino acids to host protein metabolism in a wild small mammal community

   https://doi.org/10.1111/ele.14246  

   Besser, Alexi C. ; Manlick, Philip J. ; Blevins, Christina M. ; Takacs‐Vesbach, Cristina D. ; Newsome, Seth D. ( June 2023 , Ecology Letters)

   Herbivory is a dominant feeding strategy among animals, yet herbivores are often protein limited. The gut microbiome is hypothesized to help maintain host protein balance by provisioning essential macromolecules, but this has never been tested in wild consumers. Using amino acid carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope analysis, we estimated the proportional contributions of essential amino acids (AA_ESS) synthesized by gut microbes to five co‐occurring desert rodents representing herbivorous, omnivorous and insectivorous functional groups. We found that herbivorous rodents occupying lower trophic positions (Dipodomysspp.) routed a substantial proportion (~40%–50%) of their AA_ESSfrom gut microbes, while higher trophic level omnivores (Peromyscusspp.) and insectivores (Onychomys arenicola) obtained most of their AA_ESS(~58%) from plant‐based energy channels but still received ~20% of their AA_ESSfrom gut microbes. These findings empirically demonstrate that gut microbes play a key functional role in host protein metabolism in wild animals.

    

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5. Diversity, divergence and density: How habitat and hybrid zone dynamics maintain a genomic cline in an intertidal barnacle

   https://doi.org/10.1111/jbi.14142  

   Wares, John P. ; Strand, Allan E. ; Sotka, Erik E. ( June 2021 , Journal of Biogeography)

   As within‐species genomic data have been shown useful in interpreting broader biogeographic trends, we analysed the mode of population genomic isolation involved in a well‐studied intertidal genomic cline to better understand the mechanisms maintaining it. These results were interpreted in the context of spatial variation in habitat use and availability as well as likely fitness consequences for hybridization between the two lineages.

   Pacific coast of North America.

   Arthropods (Class Maxillopoda, Order Sessilia, Family Balanidae;Balanus glandula).

   Genotype‐by‐sequencing approaches were used to generate single‐nucleotide polymorphism markers across sites sampled between southern Alaska and Southern California. Inference using standard population genomic methods, including analysis of population structure, inbreeding and linkage disequilibrium, was used to identify the steepest transitions across the largest number of loci examined. These data were put in the context of observed population density and habitat availability.

   We show that the majority of markers analysed show strong clinal transitions in a very narrow portion of the California coast. Patterns of linkage disequilibrium among markers, along with prior evidence of variation in reproductive potential by latitude and by mitochondrial lineage, suggest some reproductive isolation among the northern and southern lineages ofB. glandulathat are concordant with the drop in population density and habitat availability in central California.

   A significant clinal transition in genomic diversity is stronger and more localized than previously recognized and exhibits statistical patterns suggesting that the lineages are reproductively and phenotypically distinct in ways that may be ecologically important. As this species has been used to infer process in coastal biogeography, further study of concordant patterns will be important for advancing our understanding of this region.

    

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