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1. Transcriptional activity differentiates families of Marine Group II Euryarchaeota in the coastal ocean

   https://doi.org/10.1038/s43705-021-00002-6  

   Damashek, Julian ; Okotie-Oyekan, Aimee Oyinlade ; Gifford, Scott Michael ; Vorobev, Alexey ; Moran, Mary Ann ; Hollibaugh, James Timothy ( December 2021 , ISME Communications)

   null (Ed.)

   Abstract Marine Group II Euryarchaeota ( Candidatus Poseidoniales), abundant but yet-uncultivated members of marine microbial communities, are thought to be (photo)heterotrophs that metabolize dissolved organic matter (DOM), such as lipids and peptides. However, little is known about their transcriptional activity. We mapped reads from a metatranscriptomic time series collected at Sapelo Island (GA, USA) to metagenome-assembled genomes to determine the diversity of transcriptionally active Ca . Poseidoniales. Summer metatranscriptomes had the highest abundance of Ca . Poseidoniales transcripts, mostly from the O1 and O3 genera within Ca . Thalassarchaeaceae (MGIIb). In contrast, transcripts from fall and winter samples were predominantly from Ca . Poseidoniaceae (MGIIa). Genes encoding proteorhodopsin, membrane-bound pyrophosphatase, peptidase/proteases, and part of the ß-oxidation pathway were highly transcribed across abundant genera. Highly transcribed genes specific to Ca . Thalassarchaeaceae included xanthine/uracil permease and receptors for amino acid transporters. Enrichment of Ca . Thalassarchaeaceae transcript reads related to protein/peptide, nucleic acid, and amino acid transport and metabolism, as well as transcript depletion during dark incubations, provided further evidence of heterotrophic metabolism. Quantitative PCR analysis of South Atlantic Bight samples indicated consistently abundant Ca . Poseidoniales in nearshore and inshore waters. Together, our data suggest that Ca . Thalassarchaeaceae are important photoheterotrophs potentially linking DOM and nitrogen cycling in coastal waters. 

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2. Leave no stone unturned: individually adapted xerotolerant Thaumarchaeota sheltered below the boulders of the Atacama Desert hyperarid core

   https://doi.org/10.1186/s40168-021-01177-9  

   Hwang, Yunha ; Schulze-Makuch, Dirk ; Arens, Felix L. ; Saenz, Johan S. ; Adam, Panagiotis S. ; Sager, Christof ; Bornemann, Till L. V. ; Zhao, Weishu ; Zhang, Ying ; Airo, Alessandro ; et al ( November 2021 , Microbiome)

   The hyperarid core of the Atacama Desert is an extremely harsh environment thought to be colonized by only a few heterotrophic bacterial species. Current concepts for understanding this extreme ecosystem are mainly based on the diversity of these few species, yet a substantial area of the Atacama Desert hyperarid topsoil is covered by expansive boulder accumulations, whose underlying microbiomes have not been investigated so far. With the hypothesis that these sheltered soils harbor uniquely adapted microbiomes, we compared metagenomes and geochemistry between soils below and beside boulders across three distantly located boulder accumulations in the Atacama Desert hyperarid core.

   Genome-resolved metagenomics of eleven samples revealed substantially different microbial communities in soils below and beside boulders, despite the presence of shared species. Archaea were found in significantly higher relative abundance below the boulders across all samples within distances of up to 205 km. These key taxa belong to a novel genus of ammonia-oxidizingThaumarchaeota,CandidatusNitrosodeserticola. We resolved eight mid-to-high quality genomes of this genus and used comparative genomics to analyze its pangenome and site-specific adaptations.Ca.Nitrosodeserticola genomes contain genes for ammonia oxidation, the 3-hydroxypropionate/4-hydroxybutyrate carbon fixation pathway, and acetate utilization indicating a chemolithoautotrophic and mixotrophic lifestyle. They also possess the capacity for tolerating extreme environmental conditions as highlighted by the presence of genes against oxidative stress and DNA damage. Site-specific adaptations of the genomes included the presence of additional genes for heavy metal transporters, multiple types of ATP synthases, and divergent genes for aquaporins.

   We provide the first genomic characterization of hyperarid soil microbiomes below the boulders in the Atacama Desert, and report abundant and highly adaptedThaumarchaeaotawith ammonia oxidation and carbon fixation potential.Ca.Nitrosodeserticola genomes provide the first metabolic and physiological insight into a thaumarchaeal lineage found in globally distributed terrestrial habitats characterized by various environmental stresses. We consequently expand not only the known genetic repertoire ofThaumarchaeotabut also the diversity and microbiome functioning in hyperarid ecosystems.

    

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3. The core root microbiome of Spartina alterniflora is predominated by sulfur-oxidizing and sulfate-reducing bacteria in Georgia salt marshes, USA

   https://doi.org/10.1186/s40168-021-01187-7  

   Rolando, Jose L. ; Kolton, Max ; Song, Tianze ; Kostka, Joel E. ( December 2022 , Microbiome)

   Abstract Background Salt marshes are dominated by the smooth cordgrass Spartina alterniflora on the US Atlantic and Gulf of Mexico coastlines. Although soil microorganisms are well known to mediate important biogeochemical cycles in salt marshes, little is known about the role of root microbiomes in supporting the health and productivity of marsh plant hosts. Leveraging in situ gradients in aboveground plant biomass as a natural laboratory, we investigated the relationships between S. alterniflora primary productivity, sediment redox potential, and the physiological ecology of bulk sediment, rhizosphere, and root microbial communities at two Georgia barrier islands over two growing seasons. Results A marked decrease in prokaryotic alpha diversity with high abundance and increased phylogenetic dispersion was found in the S. alterniflora root microbiome. Significantly higher rates of enzymatic organic matter decomposition, as well as the relative abundances of putative sulfur (S)-oxidizing, sulfate-reducing, and nitrifying prokaryotes correlated with plant productivity. Moreover, these functional guilds were overrepresented in the S. alterniflora rhizosphere and root core microbiomes. Core microbiome bacteria from the Candidatus Thiodiazotropha genus, with the metabolic potential to couple S oxidation with C and N fixation, were shown to be highly abundant in the root and rhizosphere of S. alterniflora . Conclusions The S. alterniflora root microbiome is dominated by highly active and competitive species taking advantage of available carbon substrates in the oxidized root zone. Two microbially mediated mechanisms are proposed to stimulate S. alterniflora primary productivity: (i) enhanced microbial activity replenishes nutrients and terminal electron acceptors in higher biomass stands, and (ii) coupling of chemolithotrophic S oxidation with carbon (C) and nitrogen (N) fixation by root- and rhizosphere-associated prokaryotes detoxifies sulfide in the root zone while potentially transferring fixed C and N to the host plant. 

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4. Genomics, Exometabolomics, and Metabolic Probing Reveal Conserved Proteolytic Metabolism of Thermoflexus hugenholtzii and Three Candidate Species From China and Japan

   https://doi.org/10.3389/fmicb.2021.632731  

   Thomas, Scott C. ; Payne, Devon ; Tamadonfar, Kevin O. ; Seymour, Cale O. ; Jiao, Jian-Yu ; Murugapiran, Senthil K. ; Lai, Dengxun ; Lau, Rebecca ; Bowen, Benjamin P. ; Silva, Leslie P. ; et al ( May 2021 , Frontiers in Microbiology)

   Thermoflexus hugenholtzii JAD2 T , the only cultured representative of the Chloroflexota order Thermoflexales , is abundant in Great Boiling Spring (GBS), NV, United States, and close relatives inhabit geothermal systems globally. However, no defined medium exists for T. hugenholtzii JAD2 T and no single carbon source is known to support its growth, leaving key knowledge gaps in its metabolism and nutritional needs. Here, we report comparative genomic analysis of the draft genome of T. hugenholtzii JAD2 T and eight closely related metagenome-assembled genomes (MAGs) from geothermal sites in China, Japan, and the United States, representing “ Candidatus Thermoflexus japonica,” “ Candidatus Thermoflexus tengchongensis,” and “ Candidatus Thermoflexus sinensis.” Genomics was integrated with targeted exometabolomics and 13 C metabolic probing of T. hugenholtzii . The Thermoflexus genomes each code for complete central carbon metabolic pathways and an unusually high abundance and diversity of peptidases, particularly Metallo- and Serine peptidase families, along with ABC transporters for peptides and some amino acids. The T. hugenholtzii JAD2 T exometabolome provided evidence of extracellular proteolytic activity based on the accumulation of free amino acids. However, several neutral and polar amino acids appear not to be utilized, based on their accumulation in the medium and the lack of annotated transporters. Adenine and adenosine were scavenged, and thymine and nicotinic acid were released, suggesting interdependency with other organisms in situ . Metabolic probing of T. hugenholtzii JAD2 T using 13 C-labeled compounds provided evidence of oxidation of glucose, pyruvate, cysteine, and citrate, and functioning glycolytic, tricarboxylic acid (TCA), and oxidative pentose-phosphate pathways (PPPs). However, differential use of position-specific 13 C-labeled compounds showed that glycolysis and the TCA cycle were uncoupled. Thus, despite the high abundance of Thermoflexus in sediments of some geothermal systems, they appear to be highly focused on chemoorganotrophy, particularly protein degradation, and may interact extensively with other microorganisms in situ . 

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5. Ecophysiology of the Cosmopolitan OM252 Bacterioplankton ( Gammaproteobacteria )

   https://doi.org/10.1128/mSystems.00276-21  

   Savoie, Emily R. ; Lanclos, V. Celeste ; Henson, Michael W. ; Cheng, Chuankai ; Getz, Eric W. ; Barnes, Shelby J. ; LaRowe, Douglas E. ; Rappé, Michael S. ; Thrash, J. Cameron ( June 2021 , mSystems)

   Poretsky, Rachel (Ed.)

   ABSTRACT Among the thousands of species that comprise marine bacterioplankton communities, most remain functionally obscure. One key cosmopolitan group in this understudied majority is the OM252 clade of Gammaproteobacteria . Although frequently found in sequence data and even previously cultured, the diversity, metabolic potential, physiology, and distribution of this clade has not been thoroughly investigated. Here, we examined these features of OM252 bacterioplankton using a newly isolated strain and genomes from publicly available databases. We demonstrated that this group constitutes a globally distributed novel genus (“ Candidatus Halomarinus”), sister to Litoricola , comprising two subclades and multiple distinct species. OM252 organisms have small genomes (median, 2.21 Mbp) and are predicted obligate aerobes capable of alternating between chemoorganoheterotrophic and chemolithotrophic growth using reduced sulfur compounds as electron donors. Subclade I genomes encode genes for the Calvin-Benson-Bassham cycle for carbon fixation. One representative strain of subclade I, LSUCC0096, had extensive halotolerance and a mesophilic temperature range for growth, with a maximum rate of 0.36 doublings/h at 35°C. Cells were curved rod/spirillum-shaped, ∼1.5 by 0.2 μm. Growth yield on thiosulfate as the sole electron donor under autotrophic conditions was roughly one-third that of heterotrophic growth, even though calculations indicated similar Gibbs energies for both catabolisms. These phenotypic data show that some “ Ca. Halomarinus” organisms can switch between serving as carbon sources or sinks and indicate the likely anabolic cost of lithoautotrophic growth. Our results thus provide new hypotheses about the roles of these organisms in global biogeochemical cycling of carbon and sulfur. IMPORTANCE Marine microbial communities are teeming with understudied taxa due to the sheer numbers of species in any given sample of seawater. One group, the OM252 clade of Gammaproteobacteria , has been identified in gene surveys from myriad locations, and one isolated organism has even been genome sequenced (HIMB30). However, further study of these organisms has not occurred. Using another isolated representative (strain LSUCC0096) and publicly available genome sequences from metagenomic and single-cell genomic data sets, we examined the diversity within the OM252 clade and the distribution of these taxa in the world’s oceans, reconstructed the predicted metabolism of the group, and quantified growth dynamics in LSUCC0096. Our results generate new knowledge about the previously enigmatic OM252 clade and point toward the importance of facultative chemolithoautotrophy for supporting some clades of ostensibly “heterotrophic” taxa. 

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