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Ultra-small prokaryotes were prevalent across diverse aquifer lithologies and anoxic to oxic groundwatersWe used 16S rRNA gene amplicons to assess microbial community composition in 81 groundwater samples. Samples were collected from 59 wells over 10 aquifers in four geographic regions, separated by over a thousand kilometers, and encompassed wide-ranging aquifer chemistries and lithologies (Fig. 1a), comprising primarily shallow sandy-gravel aquifers, but also sand/silt, gravel/peat, volcanic (basalt, ignimbrite) and shell-bed aquifers (Table S1). A large portion of microbial community diversity comprised ultra-small groups of prokaryotes (Fig. 1b). Out of 52,553 OTUs, 21.8% (or 18.4% of 46,713 ASVs) were assigned to seven ultra-small microbial phyla (when considering CPR as the single Patescibacteria phylum). These comprised the bacterial phyla Patescibacteria and Dependentiae, and archaeal DPANN radiation. Altiarchaeota was included in DPANN as previously suggested [63, 64], although its taxonomic placement is uncertain due to genomic under-sampling [65, 66].Fig. 1: Distribution and abundance of ultra-small prokaryotes across groundwater sites.a Distribution of groundwater samples along DOC (0–26 g/m3), DO (0.37–7.5 g/m3) and nitrate-N (0.45–12.6 g/m3) concentrations scaled between 0 and 100. b Top plot: Richness of ultra-small prokaryote variants (rarefied ASVs) at each site. Middle plot: Proportion of ultra-small prokaryotes compared with the total microbial communities (black bars = OTUs, grey crosses = ASVs). Samples are ordered from least to most abundant. Lower plot: Phylum-level breakdown of amplicon based-relative abundance of Patescibacteria, Dependentiae and DPANN archaea (bottom). Symbol bars indicate aquifer lithology (top symbol bar), and oxygen content (lower symbol bar) with dark to light blue shading representing anoxic, suboxic, dysoxic to oxic groundwater. c Class-level rank abundance curve showing the average relative abundance of each genome across sites. The center line of each boxplot represents the median; the top and bottom lines are the first and third quartiles, respectively; and the whiskers show 1.5 times the interquartile range.Full size imageUltra-small prokaryotes were detected in all samples, regardless of lithology, chemistry or geography. They have also been reported from several aquifers and lithologies in the USA (sandy gravel, agriculturally-impacted river sediment, mixed marine sedimentary/metasedimentary rocks, plutonic rock, and sandstone [10, 18, 19, 22], and from a carbonate rock aquifer system in Germany [67, 68]. Collectively these findings demonstrate that ultra-small microorganisms are geographically widespread across diverse aquifer lithologies. Moreover, while ultra-small microorganisms have mostly been detected in anoxic environments [69,70,71,72] or cultivated under anoxic conditions [15, 25], we found representatives in all oxic groundwaters ( >3 mg/L DO) [73] (54/81 samples, Table S1). A few members of DPANN and Patescibacteria lineages have previously been detected in oxic environments [28, 67, 68, 74, 75], suggesting a degree of oxygen tolerance (genetic evidence presented below) or that these organisms are concentrated in anoxic niches within the aquifer substrate.The relative abundance of ultra-small microorganisms was highly variable across the studied aquifers, ranging from 0.04% to 22% of all bacterial and archaeal 16S rRNA gene sequences (7.2% average ±5.5% standard deviation; Fig. 1b). Samples with low relative abundances of ultra-small microorganisms (lower than the average) had overall lower alpha diversity (Shannon diversity indices and OTU or ASV richness) and were mostly from volcanic aquifer sites (Fig. 1b; Table S2). At the phylum level, Patescibacteria and Nanoarchaeota tended to dominate groundwater ultra-small communities (Fig. 1b). However, we found that ultra-small species level diversity overall was considerable with up to 1429 unique OTUs in a single groundwater sample (or up to 653 variants via the more conservative ASV method) (Table S2). Rarefaction curves show most variant diversity was captured across all samples, with curve slopes equaling zero (or approaching zero post rarefaction) (Fig. S1; Table S2). Finally, our results confirm the site specificity of ultra-small prokaryotes [10], with only 16 OTUs common across ≥50% of all 81 groundwater samples, or five ASVs across ≥20% of samples (three Parcubacteria, a Ca. Uhrbacteria, and a Woesearchaeales) (Table S2).High shared phylogenetic and genomic similarity to ultra-small prokaryotes from groundwaters elsewhereTo further assess the phylogeny and assess the genomic attributes and metabolic capacities of groundwater microbial communities, we reconstructed MAGs from 16 groundwater samples (eight wells over four sites and two aquifers). The dataset comprised 7,695 MAGs, including 539 unique MAGs ( >50% complete, 90% complete) (Table S3; Fig. S2). Based on phylogenetic analysis using GTDB [7, 76], MAGs represent 51 phyla, including five ultra-small microbial phyla (Table S3; Fig. S3). The ultra-small MAGs were found at all four sites and accounted for >1/3 of all unique MAGs (216 MAGs 50–100% complete, with 76 MAGs >90% complete). MAGs included 171 assigned to Patescibacteria, six to Dependentiae, and 39 to DPANN archaea (28 Nanoarchaeota, 10 Micrarchaeota, and one Altiarchaeota; Fig. 2a, b). The high representation of ultra-small prokaryotes in the MAG dataset further highlights the prevalence, diversity and abundance of these organisms in groundwater. Consistent with previous studies [6, 9, 77], genomes of ultra-small prokaryotes were small (1 ± 0.4 Mbp on average) with a tendency towards low GC contents (Figs. 3a, S2), and possessed limited metabolic capacities, which significantly differ between ultra-small bacterial and archaeal domains (results in Supplementary Materials; Figs. 3b, S2, S4).Fig. 2: Diversity of groundwater ultra-small microbial communities.Maximum likelihood phylogenetic trees of 177 unique ultra-small bacterial MAGs (a) and 39 unique ultra-small archaeal MAGs (b) recovered in this study. Outer rings indicate the site characteristics where MAGs were enriched. Enrichment factors were calculated as (average relative abundance in oxic and planktonic ultra-small microbial communities, respectively)/(average relative abundance in anoxic-to-dysoxic or sediment-enriched microbial communities, respectively). Trees are based on either 120 concatenated bacterial marker genes or 122 concatenated archaeal marker genes from GTDB-Tk, and were rooted to other groundwater bacterial and archaeal MAGs, respectively (Table S3). Scale bars indicate the number of substitutions per site. Branch background shading denotes Patescibacteria classes (clockwise): Gracilibacteria, Saccharimonadia, UBA1384, Dojkabacteria, Microgenomatia, Doudnabacteria, ABY1, Paceibacteria_A and Paceibacteria. c Proportion of ultra-small microbial OTUs (top) and MAGs (bottom) enriched in low and high oxygen groundwater, and in planktonic and sediment-enriched samples (Table S1). Enrichment factors were calculated as described above.Full size imageFig. 3: Estimated genome size, metabolic content and novelty of groundwater ultra-small prokaryotes.a Estimated genome size of groundwater MAGs calculated as (bin size – (bin size * contamination)) / (completeness), as described by Castelle et al. [9]. Genomes of ultra-small prokaryotes are colored by phylum-level. Other microbial genomes are shown in grey. b Principal Component Analysis (PCA) based on the composition of COG metabolic categories in recovered ultra-small MAGs. c (Right) Range of all pairwise AAI values (grey) and maximum AAI values (blue) between ultra-small prokaryote MAGs recovered in this study and GTDB representative genomes for a given phylum. Red dashed lines represent the AAI range defining the same family of organisms (45–65%) [74]. The number of genomes included in this analysis is indicated for each phylum in brackets. (Left) Proportion of ultra-small prokaryotic MAGs reconstructed in this study classified at each taxonomic level using GTDB-Tk.Full size imageCompared to reference genomes (GTDB species representatives), all recovered ultra-small MAGs are predicted to be novel species [78], and almost half were novel groundwater genera (Fig. 3c, results in Supplementary Materials). Most shared the highest affinity matches with other ultra-small genomes derived from aquifers elsewhere (e.g., in the USA), indicating niche adaptation within these lineages (although ultra-small MAGs from these groundwater ecosystems are over-represented in the GTDB database). Niche-specific phylogenetic conservation among geographically distant microorganisms in groundwater has likewise been reported among geographically distant anammox bacteria in groundwater [30].Ultra-small microbial communities were structured by geography, lithology, and dissolved oxygen concentrationsWhile ultra-small prokaryotes were ubiquitous in groundwater, and overall highly similar to those found in groundwater at different global locations, community compositions varied across sites. To investigate environmental factors (Table S1) influencing ultra-small community composition, we performed distance-based redundancy analysis (Fig. 4a). DO, pH, nitrate-N, sulfate, and DOC were significantly associated with differences in the distribution of 16S rRNA gene amplicon sequences annotated as Patescibacteria, Dependentiae and DPANN (permutation test, p  More

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Quantitative Biodiversity Dynamics, Ecology and Biodiversity, Utrecht University Botanic Gardens, Utrecht University, Padualaan 8, Utrecht, 3584 CH, The NetherlandsEdwin PosNaturalis Biodiversity Center, PO Box 9517, Leiden, 2300 RA, The NetherlandsEdwin Pos, Olaf S. Bánki, Paul Maas, Tinde R. van Andel & Hans ter SteegeCoordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia – INPA, Av. André Araújo, 2936, Petrópolis, Manaus, AM, 69067-375, BrazilLuiz de Souza Coelho, Diogenes de Andrade Lima Filho, Iêda Leão Amaral, Francisca Dionízia de Almeida Matos, Mariana Victória Irume, Maria Pires Martins, José Ferreira Ramos, Juan Carlos Montero, Charles Eugene Zartman, Henrique Eduardo Mendonça Nascimento, Juan David Cardenas Revilla, Flávia R. C. 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ComiskeyCenter for Conservation and Sustainability, Smithsonian Conservation Biology Institute, 1100 Jefferson Dr. SW, Suite 3123, Washington, DC, 20560-0705, USAJames A. Comiskey, Alfonso Alonso, Francisco Dallmeier & Reynaldo Linares-PalominoDepartment of Global Ecology, Carnegie Institution for Science, 260 Panama St., Stanford, CA, 94305, USAFreddie DraperUniversidade Federal do Amapá, Ciências Ambientais, Rod. Juscelino Kubitschek km2, Macapá, AP, 68902-280, BrazilJosé Julio de Toledo & Renato Richard HilárioDepartment of Integrative Biology, University of California, Berkeley, CA, 94720-3140, USAGabriel Damasco, Paul V. A. Fine & Italo MesonesBiologia Vegetal, Universidade Estadual de Campinas, Caixa Postal 6109, Campinas, SP, 13.083-970, BrazilNállarett DávilaDepartment of Ecology and Evolutionary Biology, Cornell University, Corson Hall, 215 Tower Road, Ithaca, NY, 14850, USARoosevelt García-VillacortaPeruvian Center for Biodiversity and Conservation (PCBC), Iquitos, PeruRoosevelt García-VillacortaDepartment of Ecology, University of Brasilia, Brasilia, DF, 70904-970, BrazilAline LopesICNHS, Federal University of Mato Grosso, Av. Alexandre Ferronato 1200, Setor Industrial, Sinop, MT, 78.557-267, BrazilJanaína Costa Noronha, Flávia Rodrigues Barbosa, Rainiellen de Sá Carpanedo & Domingos de Jesus RodriguesNatural Capital and Plant Health, Royal Botanic Gardens, Kew, Richmond, TW9 3AB, Surrey, UKThaise Emilio & William MillikenPrograma de Pós-Graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia – INPA, Av. 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GomesFaculty of Natural Sciences, Department of Life Sciences, Imperial College London, South Kensington Campus, Silwood ParkLondon, SW7 2AZ, UKJon LloydEcosistemas, Biodiversidad y Conservación de Especies, Universidad Estatal Amazónica, Km. 2 1/2 Vía a Tena (Paso Lateral), Puyo, Pastaza, EcuadorDavid NeillMuseo de Historia Natural Noel Kempff Mercado, Universidad Autónoma Gabriel Rene Moreno, Avenida Irala 565 Casilla Post Al 2489, Santa Cruz, Santa Cruz, BoliviaAlejandro Araujo-Murakami, Luzmila Arroyo & Daniel VillarroelDepartamento de Genética, Ecologia e Evolução, Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Av. Antônio Carlos, 6627 Pampulha, Belo Horizonte, MG, 31270-901, BrazilFernanda Antunes CarvalhoDepartment of Biology, University of Miami, Coral Gables, FL, 33146, USAKenneth J. FeeleyFairchild Tropical Botanic Garden, Coral Gables, FL, 33156, USAKenneth J. FeeleyInstituto de Biociências – Dept. 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PeresDireccíon de Evaluación Forestal y de Fauna Silvestre, Av. Javier Praod Oeste 693, Magdalena del Mar, PeruBoris Eduardo Villa ZegarraEscuela de Biología Herbario Alfredo Paredes, Universidad Central, Ap. Postal 17.01.2177, Quito, Pichincha, EcuadorCarlos CerónDepartment of Biological Sciences, Humboldt State University, 1 Harpst Street, Arcata, CA, 95521, USATerry W. HenkelMuseu Universitário / Centro de Ciências Biológicas e da Natureza / Laboratório de Botânica e Ecologia Vegetal, Universidade Federal do Acre, Rio Branco, AC, 69915-559, BrazilMarcos SilveiraInstitute of Biological and Health Sciences, Federal University of Alagoas, Av. Lourival Melo Mota, s/n, Tabuleiro do Martins, Maceio, AL, 57072-970, BrazilJuliana StroppIwokrama International Centre for Rain Forest Conservation and Development, Georgetown, GuyanaRaquel Thomas-CaesarNew York Botanical Garden, 2900 Southern Blvd, Bronx, New York, NY, 10458-5126, USADoug DalySchool of Geosciences, University of Edinburgh, 201 Crew Building, King’s Buildings, Edinburgh, EH9 3JN, UKKyle G. DexterTropical Diversity Section, Royal Botanic Garden Edinburgh, 20a Inverleith Row, Edinburgh, EH3 5LR, Scotland, UKKyle G. Dexter & Toby PenningtonServicios de Biodiversidad EIRL, Jr. Independencia 405, Iquitos, Loreto, 784, PeruMarcos Ríos Paredes, Hilda Paulette Dávila Doza, George Pepe Gallardo Gonzales & Linder Felipe Mozombite PintoHerbario Nacional de Bolivia, Universitario UMSA, Casilla 10077 Correo Central, La Paz, La Paz, BoliviaAlfredo FuentesCenter for Conservation and Sustainable Development, Missouri Botanical Garden, P.O. Box 299, St. Louis, MO, 63166-0299, USAAlfredo Fuentes, J. Sebastián Tello & William Farfan-RiosUniversidad Nacional de Jaén, Carretera Jaén San Ignacio Km 23, Jaén, Cajamarca, 06801, PeruJosé Luis Marcelo PenaBiology Department and Center for Energy, Environment and Sustainability, Wake Forest University, 1834 Wake Forest Rd, Winston Salem, NC, 27106, USAMiles R. Silman & Karina Garcia-CabreraLaboratoire Evolution et Diversité Biologique, CNRS and Université Paul Sabatier, UMR 5174 EDB, 31000, Toulouse, FranceJerome ChaveAndes to Amazon Biodiversity Program, Madre de Dios, Madre de Dios, PeruFernando Cornejo ValverdeDepartment of Anthropology, University of Texas at Austin, SAC 5.150, 2201 Speedway Stop C3200, Austin, TX, 78712, USAAnthony Di FioreFundación Puerto Rastrojo, Cra 10 No. 24-76 Oficina 1201, Bogotá, DC, ColombiaJuan Fernando PhillipsColegio de Ciencias Biológicas y Ambientales-COCIBA and Galapagos Institute for the Arts and Sciences-GAIAS, Universidad San Francisco de Quito-USFQ, Quito, Pichincha, EcuadorGonzalo Rivas-TorresDepartment of Wildlife Ecology and Conservation, University of Florida, 110 Newins-Ziegler Hall, Gainesville, FL, 32611, USAGonzalo Rivas-TorresBiosystematics Group, Wageningen University, Droevendaalsesteeg 1, Wageningen, 6708 PB, The NetherlandsTinde R. van AndelFundación Estación de Biología, Cra 10 No. 24-76 Oficina, 1201, Bogotá, DC, ColombiaPatricio von HildebrandDirection Régionale de la Guyane, ONF, Cayenne, 97300, French GuianaÉmile FontyPROTERRA, Instituto de Investigaciones de la Amazonía Peruana (IIAP), Av. A. Quiñones Km 2,5, Iquitos, Loreto, 784, PeruRicardo Zárate GómezACEER Foundation, Jirón Cusco N° 370, Puerto Maldonado, Madre de Dios, PeruTherany GonzalesDepartement EV, Muséum National d’histoire Naturelle de Paris, 16 Rue Buffon, Paris, 75005, FranceJean-Louis GuillaumetAmazon Conservation Team, Doekhieweg Oost #24, Paramaribo, SurinameBruce HoffmanInstitut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, 08193, Bellaterra, Barcelona, SpainAndré Braga JunqueiraEnvironmental Change Institute, Dyson Perrins Building, Oxford University Centre for the Environment, South Parks Road, Oxford, OX1 3QY, England, UKYadvinder MalhiInstituto de Ciencias Naturales, Universidad Nacional de Colombia, 7945, Apartado, Bogotá, DC, ColombiaAdriana Prieto & Agustín RudasInstituto de Ciência Agrárias, Universidade Federal Rural da Amazônia, Av. Presidente Tancredo Neves 2501, Belém, PA, 66.077-830, BrazilNatalino SilvaEscuela Profesional de Ingeniería Forestal, Universidad Nacional de San Antonio Abad del Cusco, Jirón San Martín 451, Puerto Maldonado, Madre de Dios, PeruCésar I. A. VelaUniversidad Autónoma del Beni José Ballivián, Campus Universitario Final, Av. Ejercito, Riberalta, Beni, BoliviaVincent Antoine VosLaboratory of Human Ecology, Instituto Venezolano de Investigaciones Científicas – IVIC, Ado 20632, Caracas, 1020A, DC, VenezuelaEgleé L. Zent & Stanford ZentCambridge University Botanic Garden, 1 Brookside., Cambridge, CB2 1JE, UKAngela CanoSchool of Agriculture and Food Sciences – ARC Centre of Excellence for Environmental Decisions CEED, The University of Queensland, St. Lucia, QLD, 4072, AustraliaDiego F. CorreaPlant Biology Department, Rua Monteiro Lobato, University of Campinas, 255, Cidade Universitária Zeferino Vaz, Barão Geraldo, Campinas, São Paulo, CEP 13083-862, BrazilBernardo Monteiro FloresResource Ecology Group, Wageningen University and Research, Droevendaalsesteeg 3a, Lumen, Building Number 100, Wageningen, Gelderland, 6708 PB, The NetherlandsMilena HolmgrenLaboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego 2000, Campos dos, Goyatacazes, RJ, 28013-620, BrazilMarcelo Trindade NascimentoInstituto de Investigaciones Para el Desarrollo Forestal (INDEFOR), Universidad de los Andes, Conjunto Forestal, Mérida, Mérida, 5101, VenezuelaHirma Ramirez-Angulo, Emilio Vilanova Torre & Armando Torres-LezamaDepartamento de Biologia, Universidade Federal do Amazonas – UFAM – Instituto de Ciências Biológicas – ICB1, Av General Rodrigo Octavio 6200, Manaus, AM, 69080-900, BrazilVeridiana Vizoni ScudellerGeoIS, el Día 369 y el Telégrafo, 3° Piso, Quito, Pichincha, EcuadorRodrigo Sierra & Milton TiradoDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109, USAMaria Natalia UmañaUniversity of Nottingham, University Park, Nottingham, NG7 2RD, UKGeertje van der HeijdenSchool of Environmental and Forest Sciences, University of Washington, Seattle, WA, 98195-2100, USAEmilio Vilanova TorreEnvironmental Science and Policy, Northern Arizona University, Flagstaff, AZ, 86011, USAOphelia WangGeography and the Environment, University of Texas at Austin, 305 E. 23Rd Street, CLA Building, Austin, TX, 78712, USAKenneth R. YoungMedio Ambiente, PLUSPRETOL, Iquitos, Loreto, PeruManuel Augusto Ahuite ReateguiThe Mauritius Herbarium, Agricultural Services, Ministry of Agro-Industry and Food Security, Reduit, 80835, MauritiusCláudia BaiderDepartment of Bioscience, Aarhus University, Building 1540 Ny Munkegade, 8000, Aarhus C, Aarhus, DenmarkHenrik BalslevLiving Earth Collaborative, Washington University in Saint Louis, St. Louis, MO, 63130, USAWilliam Farfan-RiosEscuela de Ciencias Forestales (ESFOR), Universidad Mayor de San Simon (UMSS), Sacta, Cochabamba, BoliviaCasimiro MendozaFOMABO, Manejo Forestal en Las Tierras Tropicales de Bolivia, Sacta, Cochabamba, BoliviaCasimiro MendozaTropenbos International, Lawickse Allee 11, PO Box 232, Wageningen, 6700 AE, The NetherlandsRoderick ZagtSchool of Anthropology and Conservation, University of Kent, Marlowe Building, Canterbury, Kent, CT2 7NR, UKMiguel N. AlexiadesHerbario Nacional del Ecuador, Universidad Técnica del Norte, Quito, Pichincha, EcuadorWalter Palacios CuencaInstituto de Biodiversidade e Floresta, Universidade Federal do Oeste do Pará, Rua Vera Paz, Campus Tapajós, Santarém, PA, 68015-110, BrazilDaniela PaulettoFacultad de Biologia, Universidad Nacional de la Amazonia Peruana, Pevas 5Ta Cdra, Iquitos, Loreto, PeruFreddy Ramirez Arevalo & Elvis H. Valderrama SandovalDepartment of Biology, University of Missouri, St. Louis, MO, 63121, USAElvis H. Valderrama SandovalDepartment of Biogeochemical Integration, Max-Planck-Institute for Biogeochemistry, P.O. Box 10 01 64, 07701, Jena, GermanyGerhard BoenischFunctional Biogeography, Max-Planck-Institute for Biogeochemistry, P.O. Box 10 01 64, 07701, Jena, GermanyJens KattgeDepartment of Ecology and Evolutionary Biology, UCLA, 621 Charles E. Young Drive South, Box 951606, Los Angeles, CA, 90095, USANathan KraftE.T.P. and H.T.S. designed the study. E.T.P. performed analyses and took the lead in writing the manuscript, H.T.S. supervised the writing and provided regular feedback both for the manuscript and the interpretation of the results. All other authors provided feedback on the manuscript and provided their data from the Amazon Tree Diversity Network or trait data. Authors E.T.P. to L.V.G. provided tree inventory data, authors G.B., J.K., N.K., A.L., K.M., G.P., L.P. provided data on functional traits, C.B., J.L., A.A.O. and H.T.S. provided both tree inventory and functional trait data. More

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