Pangenomics Analysis Reveals Diversification of Enzyme Families and Niche Specialization in Globally Abundant SAR202 Bacteria DOI Creative Commons
Jimmy H. Saw, Takuro Nunoura, Miho Hirai

et al.

mBio, Journal Year: 2020, Volume and Issue: 11(1)

Published: Jan. 6, 2020

It has been hypothesized that the abundant heterotrophic ocean bacterioplankton in SAR202 clade of phylum Chloroflexi evolved specialized metabolisms for oxidation organic compounds are resistant to microbial degradation via common metabolic pathways. Expansions paralogous enzymes were reported and implicated hypothetical metabolism involving monooxygenase dioxygenase enzymes. In proposed schemes, paralogs serve purpose diversifying range molecules cells can utilize. To further explore evolution metabolism, we reconstructed single amplified genomes metagenome-assembled from locations around world included deepest trenches. an analysis 122 seven subclades spanning diversity, observed additional evidence paralog expansions correlated with evolutionary history, as well specialization. Consistent previous reports, families flavin-dependent monooxygenases mainly group III genomes, prevalent those VII. We found I encode racemases enolase superfamily, which propose resist biological because chiral complexity. Supporting conclusion indicate specialization, fragment recruitment fluorescent situ hybridization (FISH) phylogenetic probes showed indigenous different depths geographical regions. Surprisingly, some surface waters contained rhodopsin genes, altering our understanding ecological role species stratified water columns.IMPORTANCE The oceans contain estimated 662 Pg C form dissolved matter (DOM). Information about interactions this vast resource is limited, despite broad recognition DOM turnover a major impact on global carbon cycle. explain patterns marine bacteria, pathways schemes suggest new classes could be important distribution throughout biosphere. These genome-based will remain until experimental cell biology gathered test them. Our findings also fundamentally change ecology showing metabolically diverse variants these occupy niches all not relegated dark ocean.

Language: Английский

Deep mitochondrial origin outside the sampled alphaproteobacteria DOI Open Access
Joran Martijn, Julian Vosseberg, Lionel Guy

et al.

Nature, Journal Year: 2018, Volume and Issue: 557(7703), P. 101 - 105

Published: April 20, 2018

Language: Английский

Citations

347

Deep ocean metagenomes provide insight into the metabolic architecture of bathypelagic microbial communities DOI Creative Commons
Silvia G. Acinas, Pablo Sánchez, Guillem Salazar

et al.

Communications Biology, Journal Year: 2021, Volume and Issue: 4(1)

Published: May 21, 2021

Abstract The deep sea, the largest ocean’s compartment, drives planetary-scale biogeochemical cycling. Yet, functional exploration of its microbial communities lags far behind other environments. Here we analyze 58 metagenomes from tropical and subtropical oceans to generate Malaspina Gene Database. Free-living or particle-attached lifestyles drive differences in bathypelagic prokaryotic communities, regardless their biogeography. Ammonia CO oxidation pathways are enriched free-living dissimilatory nitrate reduction ammonium H 2 particle-attached, while Calvin Benson-Bassham cycle is most prevalent inorganic carbon fixation pathway both size fractions. Reconstruction Deep Metagenome-Assembled Genomes reveals unique non-cyanobacterial diazotrophic bacteria chemolithoautotrophic prokaryotes. widespread potential grow autotrophically heterotrophically suggests that mixotrophy an ecologically relevant trait ocean. These results expand our understanding structure metabolic capabilities Earth aquatic ecosystem.

Language: Английский

Citations

161

Novel Chloroflexi genomes from the deepest ocean reveal metabolic strategies for the adaptation to deep-sea habitats DOI Creative Commons
Rulong Liu, Xing Wei, Weizhi Song

et al.

Microbiome, Journal Year: 2022, Volume and Issue: 10(1)

Published: May 10, 2022

The deep sea harbors the majority of microbial biomass in ocean and is a key site for organic matter (OM) remineralization storage biosphere. Microbial metabolism greatly controlled by generally depleted but periodically fluctuating supply OM. Currently, little known about metabolic potentials dominant deep-sea microbes to cope with variable OM inputs, especially those living hadal trenches-the deepest part ocean.In this study, we report first extensive examination sediment Chloroflexi, phylum trenches global ocean. In total, 62 metagenome-assembled-genomes (MAGs) were reconstructed from nine metagenomic datasets derived sediments Mariana Trench. These MAGs represent six novel species, four genera, one family, order within classes Anaerolineae Dehalococcoidia. Fragment recruitment showed that these are globally distributed waters surface sediments, transcriptomic analysis indicated their situ activities. Metabolic reconstruction Chloroflexi mainly had heterotrophic lifestyle, potential degrade wide range carbon, sulfur, halogenated compounds. Our results revealed time harbor pathways complete hydrolytic or oxidative degradation various recalcitrant OM, including aromatic compounds (e.g., benzoate), polyaromatic hydrocarbons fluorene), polychlorobiphenyl 4-chlorobiphenyl), organochlorine chloroalkanes, chlorocyclohexane). Moreover, organisms synthesize energy trehalose) regulatory modules respond changes nutrient conditions. traits suggest may follow "feast-or-famine" strategy, i.e., preferentially consume labile store intracellularly under OM-rich conditions, utilize stored survival OM-limited condition.This study expands current knowledge on strategies deep-ocean Chlorolfexi highlights significance halogen cycles. plasticity likely provides advantages heterogenic inputs Video Abstract.

Language: Английский

Citations

73

Hidden in plain sight—highly abundant and diverse planktonic freshwater Chloroflexi DOI Creative Commons
Maliheh Mehrshad, Michaela M. Salcher, Yusuke Okazaki

et al.

Microbiome, Journal Year: 2018, Volume and Issue: 6(1)

Published: Oct. 2, 2018

Representatives of the phylum Chloroflexi, though reportedly highly abundant in extensive deep water habitats both marine (SAR202 up to 30% total prokaryotes) and freshwater (CL500-11 26% prokaryotes), remain uncultivated uncharacterized. There are few metagenomic studies on Chloroflexi representatives, while pelagic community is largely unknown except for a single metagenome-assembled genome CL500-11. Here, we provide first examination composition this cosmopolitan range (176 datasets) highlight impact salinity depth their phylogenomic composition. Reconstructed genomes (53 total) perspective phylogeny, metabolism, distribution three novel classes two family-level taxa within Chloroflexi. We unraveled remarkable genomic diversity representatives that thrive not only hypolimnion as previously suspected, but also epilimnion. Our results suggest lake provides globally stable habitat reflected lower species among hypolimnion-specific CL500-11 TK10 clusters distantly related lakes compared higher epilimnion-specific SL56 cluster. Cell volume analyses show largest prokaryotic cells column with biomass abundance ratio they significantly contribute carbon flow. Metabolic insights indicate participation JG30-KF-CM66 global cobalamin production via cobinamide salvage pathway. Extending comparisons brackish suggests major influencer deep-dwelling (SAR202) (CL500-11) counterparts intermediate salinity; however, harbor most phylogenetically diverse reside epi- hypolimnion.

Language: Английский

Citations

154

Linking metagenomics to aquatic microbial ecology and biogeochemical cycles DOI Creative Commons
Hans‐Peter Grossart, Ramón Massana, Katherine D. McMahon

et al.

Limnology and Oceanography, Journal Year: 2019, Volume and Issue: 65(S1)

Published: Nov. 20, 2019

Abstract Microbial communities are essential components of aquatic ecosystems through their contribution to food web dynamics and biogeochemical processes. Aquatic microbial diversity is immense a general challenge understand how metabolism interactions single organisms shape community ecosystem‐scale transformations. Metagenomic approaches have developed rapidly, proven be powerful in linking In this review, we provide an overview metagenomic approaches, followed by discussion on some recent insights they provided, including those special issue. These include the discovery new taxa metabolisms microbiomes, into assembly functional ecology as well evolutionary processes shaping genomes influence human activities microbiomes. Given that metagenomics can now considered mature technology where data generation descriptive analyses relatively routine informative, then discuss metagenomic‐enabled research avenues further link integration well‐designed ecological experiments, use inform validate metabolic models, pressing need for ecologically relevant model simple systems better interpret taxonomic information integrated metagenomes. will contribute more mechanistic predictive understanding links between cycles. Owing rapid climate change impacts ecosystems, urgency such has never been greater.

Language: Английский

Citations

128

Genomic evidence for the degradation of terrestrial organic matter by pelagic Arctic Ocean Chloroflexi bacteria DOI Creative Commons

David Colatriano,

Patricia Q. Tran, Céline Guéguen

et al.

Communications Biology, Journal Year: 2018, Volume and Issue: 1(1)

Published: June 29, 2018

The Arctic Ocean currently receives a large supply of global river discharge and terrestrial dissolved organic matter. Moreover, an increase in freshwater runoff riverine transport matter to the is predicted consequence thawing permafrost increased precipitation. fate humic-rich material its impact on marine carbon cycle are largely unknown. Here, metagenomic survey Canada Basin Western showed that pelagic Chloroflexi from replete with aromatic compound degradation genes, acquired part by lateral transfer bacteria. Our results imply have capacity use their role may changing hydrological cycle.

Language: Английский

Citations

103

Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico “Dead Zone” DOI Creative Commons
J. Cameron Thrash,

Kiley W. Seitz,

Brett J. Baker

et al.

mBio, Journal Year: 2017, Volume and Issue: 8(5)

Published: Sept. 13, 2017

Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called "dead zones," are increasing in number and severity around the globe with deleterious effects on ecology economics. One of largest these coastal dead zones occurs continental shelf northern Gulf Mexico (nGOM), which results from eutrophication-enhanced bacterioplankton respiration strong stratification. Previous research this zone revealed presence multiple cosmopolitan lineages eluded cultivation, thus their metabolic roles ecosystem remain unknown. We used a coupled shotgun metagenomic metatranscriptomic approach determine potential Group II Euryarchaeota, SAR406, SAR202. recovered high-quality, nearly complete genomes all three groups as well candidate phyla usually associated anoxic environments-Parcubacteria (OD1) Peregrinibacteria Two additional putative assignments ACD39 PAUC34f supplement contributions by uncultivated taxa. Our indicate active metabolism groups, including prevalent aerobic respiration, concurrent expression genes for nitrate reduction SAR406 SAR202, dissimilatory nitrite ammonia sulfur SAR406. also report variety heterotrophic carbon processing mechanisms, degradation complex carbohydrate compounds ACD39, PAUC34f. Together, data help constrain nGOM during periods DO suggest organisms breakdown organic matter.IMPORTANCE Dead receive name primarily eukaryotic macrobiota (demersal fish, shrimp, etc.) key fisheries. Excess nutrients contributed anthropogenic activity such fertilizer runoff result algal blooms therefore ample new microbial metabolism. Combined stratification, reduces bottom waters levels unfit many animals (termed hypoxia). The remains one eutrophication-driven hypoxic world, yet despite its model study system, metabolisms underlying resulting phenomenon-many occur poorly understood lineages-have received only preliminary study. work details gene across several sites nGOM, improving our understanding biogeochemical cycling mediated "microbial dark matter" taxa hypoxia.

Language: Английский

Citations

99

Metagenomes Reveal Global Distribution of Bacterial Steroid Catabolism in Natural, Engineered, and Host Environments DOI Creative Commons
Johannes Holert, Erick Cardenas,

Lee Bergstrand

et al.

mBio, Journal Year: 2018, Volume and Issue: 9(1)

Published: March 7, 2018

ABSTRACT Steroids are abundant growth substrates for bacteria in natural, engineered, and host-associated environments. This study analyzed the distribution of aerobic 9,10-seco steroid degradation pathway 346 publically available metagenomes from diverse Our results show that steroid-degrading globally distributed prevalent particular environments, such as wastewater treatment plants, soil, plant rhizospheres, marine environment, including sponges. Genomic signature-based sequence binning recovered 45 metagenome-assembled genomes containing a majority genes. Only Actinobacteria Proteobacteria were identified degraders, but we several alpha- gammaproteobacterial lineages not previously known to degrade steroids. Actino- proteobacterial degraders coexisted wastewater, while soil rhizosphere samples contained mostly actinobacterial ones. Actinobacterial found deep ocean samples, ones other Isolation sponges confirmed their presence. Phylogenetic analysis key proteins suggested biochemical novelty shows ecological significance well taxonomic diversity bacterial has so far been largely underestimated, especially environment. IMPORTANCE Microbial is critical process biomass decomposition natural removal important pollutants during treatment, pathogenesis associated with tuberculosis bacteria. To date, microbial was mainly studied few model organisms, remained unexplored. provides first environments via bioinformatic an extensive metagenome data set. We underestimated. greatly expands our evolutionary understanding degradation.

Language: Английский

Citations

92

Marine Sponges as Chloroflexi Hot Spots: Genomic Insights and High-Resolution Visualization of an Abundant and Diverse Symbiotic Clade DOI Creative Commons
Kristina Bayer, Martin T. Jahn, Beate M. Slaby

et al.

mSystems, Journal Year: 2018, Volume and Issue: 3(6)

Published: Oct. 30, 2018

Members of the widespread bacterial phylum Chloroflexi can dominate high-microbial-abundance (HMA) sponge microbiomes. In Sponge Microbiome Project, sequences amounted to 20 30% total microbiome certain HMA genera with classes/clades SAR202, Caldilineae, and Anaerolineae being most prominent. We performed metagenomic single-cell genomic analyses elucidate functional gene repertoire symbionts Aplysina aerophoba. Eighteen draft genomes were reconstructed placed into phylogenetic context which six investigated in detail. Common features related central energy carbon converting pathways, amino acid fatty metabolism, respiration. Clade-specific metabolic included a massively expanded for carbohydrate degradation Caldilineae genomes, but only utilization by SAR202. While import cofactors vitamins, SAR202 harbor genes encoding components involved cofactor biosynthesis. A number relevant symbiosis further identified, including CRISPR-Cas systems, eukaryote-like repeat proteins, secondary metabolite clusters. visualized extracellular matrix at ultrastructural resolution fluorescence situ hybridization-correlative light electron microscopy (FISH-CLEM) method. Carbohydrate potential was reported previously "Candidatus Poribacteria" SAUL, typical sponges, we propose here that collectively engage dissolved organic matter, both labile recalcitrant. Thus, microbes may not provide nutrients host, they also contribute matter (DOM) recycling primary productivity reef ecosystems via pathway termed loop. IMPORTANCEChloroflexi represent widespread, yet enigmatic few cultivated members. used approaches characterize marine sponges. The results this study suggest clade-specific specialization have from seawater. Considering abundance dominance sponges many benthic environments, predict role biogeochemical cycles is larger than thought.

Language: Английский

Citations

90

Archaea dominate oxic subseafloor communities over multimillion-year time scales DOI Creative Commons
Aurèle Vuillemin, Scott D. Wankel, Ömer K. Coskun

et al.

Science Advances, Journal Year: 2019, Volume and Issue: 5(6)

Published: June 1, 2019

Archaea have dominated oxic subseafloor communities for millions of years by minimizing energy loss.

Language: Английский

Citations

81