Ubiquitous genome streamlined Acidobacteriota in freshwater environments
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
39544963
PubMed Central
PMC11561045
DOI
10.1093/ismeco/ycae124
PII: ycae124
Knihovny.cz E-zdroje
- Klíčová slova
- Acidiparvus, aquatic microbial ecology, freshwater lakes, genome streamlined Acidobacteriota metagenomics, genome streamlined bacteria,
- Publikační typ
- časopisecké články MeSH
Acidobacteriota are abundant in soil, peatlands, and sediments, but their ecology in freshwater environments remains understudied. UBA12189, an Acidobacteriota genus, is an uncultivated, genome-streamlined lineage with a small genome size found in aquatic environments where detailed genomic analyses are lacking. Here, we analyzed 66 MAGs of UBA12189 (including one complete genome) from freshwater lakes and rivers in Europe, North America, and Asia. UBA12189 has small genome sizes (<1.4 Mbp), low GC content, and a highly diverse pangenome. In freshwater lakes, this bacterial lineage is abundant from the surface waters (epilimnion) down to a 300-m depth (hypolimnion). UBA12189 appears to be free-living from CARD-FISH analysis. When compared to other genome-streamlined bacteria such as Nanopelagicales and Methylopumilus, genome reduction has caused UBA12189 to have a more limited metabolic repertoire in carbon, sulfur, and nitrogen metabolisms, limited numbers of membrane transporters, as well as a higher degree of auxotrophy for various amino acids, vitamins, and reduced sulfur. Despite having reduced genomes, UBA12189 encodes proteorhodopsin, complete biosynthesis pathways for heme and vitamin K2, cbb3-type cytochrome c oxidases, and heme-requiring enzymes. These genes may give a selective advantage during the genome streamlining process. We propose the new genus Acidiparvus, with two new species named "A. lacustris" and "A. fluvialis". Acidiparvus is the first described genome-streamlined lineage under the phylum Acidobacteriota, which is a free-living, slow-growing scavenger in freshwater environments.
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Giovannoni SJ, Cameron Thrash J, Temperton B. Implications of streamlining theory for microbial ecology. ISME J 2014;8:1553–65. 10.1038/ismej.2014.60 PubMed DOI PMC
Giovannoni SJ, Bibbs L, Cho JCet al. . Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 2005;438:82–5. 10.1038/nature04032 PubMed DOI
Henson MW, Lanclos VC, Faircloth BCet al. . Cultivation and genomics of the first freshwater SAR11 (LD12) isolate. ISME J 2018;12:1846–60. 10.1038/s41396-018-0092-2 PubMed DOI PMC
Giovannoni SJ, Hayakawa DH, Tripp HJet al. . The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 2008;10:1771–82. 10.1111/j.1462-2920.2008.01598.x PubMed DOI
Salcher MM, Neuenschwander SM, Posch Tet al. . The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign. ISME J 2015;9:2442–53. 10.1038/ismej.2015.55 PubMed DOI PMC
Garcia SL, McMahon KD, Martinez-Garcia Met al. . Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton. ISME J 2013;7:137–47. 10.1038/ismej.2012.86 PubMed DOI PMC
Ghai R, Mizuno CM, Picazo Aet al. . Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep 2013;3:2471. 10.1038/srep02471 PubMed DOI PMC
Ghylin TW, Garcia SL, Moya Fet al. . Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage. ISME J 2014;8:2503–16. 10.1038/ismej.2014.135 PubMed DOI PMC
Hahn MW, Schmidt J, Taipale SJet al. . Rhodoluna lacicola gen. nov., sp. nov., a planktonic freshwater bacterium with stream-lined genome. Int J Syst Evol Microbiol 2014;64:3254–63. 10.1099/ijs.0.065292-0 PubMed DOI PMC
Neuenschwander SM, Ghai R, Pernthaler Jet al. . Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria. ISME J 2018;12:185–98. 10.1038/ismej.2017.156 PubMed DOI PMC
Eichorst SA, Trojan D, Roux Set al. . Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environ Microbiol 2018;20:1041–63. 10.1111/1462-2920.14043 PubMed DOI PMC
Ward NL, Challacombe JF, Janssen PHet al. . Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 2009;75:2046–56. 10.1128/AEM.02294-08 PubMed DOI PMC
Kielak AM, Barreto CC, Kowalchuk GAet al. . The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 2016;7:744. 10.3389/fmicb.2016.00744 PubMed DOI PMC
Dyksma S, Pester M. Oxygen respiration and polysaccharide degradation by a sulfate-reducing acidobacterium. Nat Commun 2023;14:6337. 10.1038/s41467-023-42074-z PubMed DOI PMC
Kleinsteuber S, Müller FD, Chatzinotas Aet al. . Diversity and in situ quantification of Acidobacteria subdivision 1 in an acidic mining lake. FEMS Microbiol Ecol 2008;63:107–17. 10.1111/j.1574-6941.2007.00402.x PubMed DOI
Zimmermann J, Portillo MC, Serrano Let al. . Acidobacteria in freshwater ponds at Doñana national park, Spain. Microb Ecol 2012;63:844–55. 10.1007/s00248-011-9988-3 PubMed DOI
Santofimia E, González-Toril E, López-Pamo Eet al. . Microbial diversity and its relationship to physicochemical characteristics of the water in two extreme acidic pit lakes from the Iberian Pyrite Belt (SW Spain). PLoS One 2013;8:e66746. 10.1371/journal.pone.0066746 PubMed DOI PMC
Smith DJ, Kharbush JJ, Kersten RDet al. . Uptake of phytoplankton-derived carbon and cobalamins by novel Acidobacteria genera in Microcystis blooms inferred from metagenomic and metatranscriptomic evidence. Appl Environ Microbiol 2022;88:e0180321–1. 10.1128/aem.01803-21 PubMed DOI PMC
Liesack W, Bak F, Kreft JUet al. . Holophaga foetida gen. nov., sp. nov., a new, homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch Microbiol 1994;162:85–90. PubMed
Coates JD, Ellis DJ, Gaw CVet al. . Geothrix fermentans gen. nov., sp. nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. Int J Syst Evol Microbiol 1999;49:1615–22. 10.1099/00207713-49-4-1615 PubMed DOI
Parks DH, Chuvochina M, Rinke Cet al. . GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res 2022;50:D785–94. 10.1093/nar/gkab776 PubMed DOI PMC
Coleman M. Comparative Microbial Biogeochemistry in the Laurentian Great Lakes. Berkeley, CA (United States): USDOE Joint Genome Institute (JGI), 2014.
Okazaki Y, Nishimura Y, Yoshida Tet al. . Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake. Environ Microbiol 2019;21:4740–54. 10.1111/1462-2920.14816 PubMed DOI
Okazaki Y, Nakano SI, Toyoda Aet al. . Long-read-resolved, ecosystem-wide exploration of nucleotide and structural microdiversity of lake bacterioplankton genomes. mSystems 2022;7:e00433–22. 10.1128/msystems.00433-22 PubMed DOI PMC
Xing P, Tao Y, Luo Jet al. . Stratification of microbiomes during the holomictic period of Lake Fuxian, an alpine monomictic lake. Limnol Oceanogr 2020;65:S134–48. 10.1002/lno.11346 DOI
Buck M, Garcia SL, Fernandez Let al. . Comprehensive dataset of shotgun metagenomes from oxygen stratified freshwater lakes and ponds. Sci Data 2021;8:131. 10.1038/s41597-021-00910-1 PubMed DOI PMC
Smith MW, Herfort L, Rivers ARet al. . Genomic signatures for sedimentary microbial utilization of phytoplankton detritus in a fast-flowing estuary. Front Microbiol 2019;10:2475. 10.3389/fmicb.2019.02475 PubMed DOI PMC
Hamada M, Toyofuku M, Miyano Tet al. . cbb3-type cytochrome c oxidases, aerobic respiratory enzymes, impact the anaerobic life of Pseudomonas aeruginosa PAO1. J Bacteriol 2014;196:3881–9. 10.1128/JB.01978-14 PubMed DOI PMC
Mukherjee I, Salcher MM, Andrei A-Şet al. . A freshwater radiation of diplonemids. Environ Microbiol 2020;22:4658–68. 10.1111/1462-2920.15209 PubMed DOI
Chiriac MC, Bulzu PA, Andrei ASet al. . Ecogenomics sheds light on diverse lifestyle strategies in freshwater CPR. Microbiome 2022;10:1–21. 10.1186/s40168-022-01274-3 PubMed DOI PMC
Bushnell B. BBMap: A Fast, Accurate, Splice-Aware Aligner. Berkeley, CA (United States): Lawrence Berkeley National Lab.(LBNL), 2014.
Li D, Liu CM, Luo Ret al. . MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 2015;31:1674–6. 10.1093/bioinformatics/btv033 PubMed DOI
Kang DD, Li F, Kirton Eet al. . MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 2019;7:e7359. 10.7717/peerj.7359 PubMed DOI PMC
Hyatt D, Chen GL, LoCascio PFet al. . Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010;11:1–11. 10.1186/1471-2105-11-119 PubMed DOI PMC
Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol 2017;35:1026–8. 10.1038/nbt.3988 PubMed DOI
Roux S, Enault F, Hurwitz BLet al. . VirSorter: mining viral signal from microbial genomic data. PeerJ 2015;3:e985. 10.7717/peerj.985 PubMed DOI PMC
Kieft K, Zhou Z, Anantharaman K. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome 2020;8:1–23. 10.1186/s40168-020-00867-0 PubMed DOI PMC
Olm MR, Brown CT, Brooks Bet al. . dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J 2017;11:2864–8. 10.1038/ismej.2017.126 PubMed DOI PMC
Chklovski A, Parks DH, Woodcroft BJet al. . CheckM2: a rapid, scalable and accurate tool for assessing microbial genome quality using machine learning. Nat Methods 2023;20:1203–12. 10.1038/s41592-023-01940-w PubMed DOI
Li H. Fast construction of FM-index for long sequence reads. Bioinformatics 2014;30:3274–5. 10.1093/bioinformatics/btu541 PubMed DOI PMC
Bonenfant Q, Noé L, Touzet H. Porechop_ABI: discovering unknown adapters in Oxford Nanopore technology sequencing reads for downstream trimming. Bioinform Adv 2023;3:1–4. 10.1093/bioadv/vbac085 PubMed DOI PMC
Mak QXC, Wick RR, Holt JMet al. . Polishing de novo nanopore assemblies of bacteria and eukaryotes with FMLRC2. Mol Biol Evol 2023;40:1–5. 10.1093/molbev/msad048 PubMed DOI PMC
Kolmogorov M, Bickhart DM, Behsaz Bet al. . metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat Methods 2020;17:1103–10. 10.1038/s41592-020-00971-x PubMed DOI PMC
Huang Y, Li W, Finn PWet al. . Ribosomal RNA identification in metagenomic and metatranscriptomic datasets. In: Bruijn FJ (ed.), Handbook of Molecular Microbial Ecology, Metagenomics and Complementary Approaches. Vol. 1, 1st edn. Hoboken: Wiley, 2011, 387–9110.1002/9781118010518.ch44 DOI
Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997;25:955–64. 10.1093/nar/25.5.955 PubMed DOI PMC
Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011;39:W29–37. 10.1093/nar/gkr367 PubMed DOI PMC
Tatusov RL, Natale DA, Garkavtsev IVet al. . The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 2001;29:22–8. 10.1093/nar/29.1.22 PubMed DOI PMC
Haft DH, Loftus BJ, Richardson DLet al. . TIGRFAMs: a protein family resource for the functional identification of proteins. Nucleic Acids Res 2001;29:41–3. 10.1093/nar/29.1.41 PubMed DOI PMC
Mistry J, Bateman A, Finn RD. Predicting active site residue annotations in the Pfam database. BMC Bioinformatics 2007;8:1–4. 10.1186/1471-2105-8-298 PubMed DOI PMC
Kanehisa M, Sato Y, Kawashima Met al. . KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 2016;44:D457–62. 10.1093/nar/gkv1070 PubMed DOI PMC
Jones P, Binns D, Chang HYet al. . InterProScan 5: genome-scale protein function classification. Bioinformatics 2014;30:1236–40. 10.1093/bioinformatics/btu031 PubMed DOI PMC
Yin Y, Mao X, Yang Jet al. . dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2012;40:W445–51. 10.1093/nar/gks479 PubMed DOI PMC
Hauser M, Steinegger M, Söding J. MMseqs software suite for fast and deep clustering and searching of large protein sequence sets. Bioinformatics 2016;32:1323–30. 10.1093/bioinformatics/btw006 PubMed DOI
Emiola A, Oh J. High throughput in situ metagenomic measurement of bacterial replication at ultra-low sequencing coverage. Nat Commun 2018;9:4956. 10.1038/s41467-018-07240-8 PubMed DOI PMC
Chen IA, Chu K, Palaniappan Ket al. . THE IMG/M data management and analysis system v.7: content updates and new features. Nucleic Acids Res 2023;51:D723–32. 10.1093/nar/gkac976 PubMed DOI PMC
Löytynoja A. Phylogeny-aware alignment with PRANK. Methods Mol Biol 2014;1079155–70. 10.1007/978-1-62703-646-7_10 PubMed DOI
Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010;10:210–21. 10.1186/1471-2148-10-210 PubMed DOI PMC
Minh BQ, Schmidt HA, Chernomor Oet al. . IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020;37:1530–4. 10.1093/molbev/msaa015 PubMed DOI PMC
Kalyaanamoorthy S, Minh BQ, Wong TKet al. . ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017;14:587–9. 10.1038/nmeth.4285 PubMed DOI PMC
Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019;47:W256–9. 10.1093/nar/gkz239 PubMed DOI PMC
Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11:2399–406. 10.1038/ismej.2017.113 PubMed DOI PMC
Goris J, Konstantinidis KT, Klappenbach JAet al. . DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007;57:81–91. 10.1099/ijs.0.64483-0 PubMed DOI
Qin QL, Xie BB, Zhang XYet al. . A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014;196:2210–5. 10.1128/JB.01688-14 PubMed DOI PMC
Hedlund BP, Chuvochina M, Hugenholtz Pet al. . SeqCode: a nomenclatural code for prokaryotes described from sequence data. Nat Microbiol 2022;7:1702–8. 10.1038/s41564-022-01214-9 PubMed DOI PMC
Salcher MM, Schaefle D, Kaspar Met al. . Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae. ISME J 2019;13:2764–77. 10.1038/s41396-019-0471-3 PubMed DOI PMC
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013;30:772–80. 10.1093/molbev/mst010 PubMed DOI PMC
Käll L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Res 2007;35:W429–32. 10.1093/nar/gkm256 PubMed DOI PMC
Bulzu PA, Kavagutti VS, Andrei ASet al. . The evolutionary kaleidoscope of Rhodopsins. MSystems 2022;7:e00405–22. 10.1128/msystems.00405-22 PubMed DOI PMC
Mirarab S, Nguyen N, Guo Set al. . PASTA: ultra-large multiple sequence alignment for nucleotide and amino-acid sequences. J Comput Biol 2015;22:377–86. 10.1089/cmb.2014.0156 PubMed DOI PMC
Harrison KJ, Crécy-Lagard V, Zallot R. Gene graphics: a genomic neighborhood data visualization web application. Bioinformatics 2018;34:1406–8. 10.1093/bioinformatics/btx793 PubMed DOI PMC
Salcher MM, Pernthaler J, Posch T. Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12). ISME J 2011;5:1242–52. 10.1038/ismej.2011.8 PubMed DOI PMC
Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823–9. 10.1093/bioinformatics/bts252 PubMed DOI PMC
Ludwig W, Strunk O, Westram Ret al. . ARB: a software environment for sequence data. Nucleic Acids Res 2004;32:1363–71. 10.1093/nar/gkh293 PubMed DOI PMC
Quast C, Pruesse E, Yilmaz Pet al. . The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2012;41:D590–6. 10.1093/nar/gks1219 PubMed DOI PMC
Stamatakis A, Ludwig T, Meier H. RAxML-II: a program for sequential, parallel and distributed inference of large phylogenetic trees. Concurr Comput Pract Exp 2005;17:1705–23. 10.1002/cpe.954 DOI
Yilmaz LS, Parnerkar S, Noguera DR. mathFISH, a web tool that uses thermodynamics-based mathematical models for in silico evaluation of oligonucleotide probes for fluorescence in situ hybridization. Appl Environ Microbiol 2011;77:1118–22. 10.1128/AEM.01733-10 PubMed DOI PMC
Chiriac MC, Haber M, Salcher MM. Adaptive genetic traits in pelagic freshwater microbes. Environ Microbiol 2023;25:606–41. 10.1111/1462-2920.16313 PubMed DOI
Tripp HJ, Kitner JB, Schwalbach MSet al. . SAR11 marine bacteria require exogenous reduced Sulphur for growth. Nature 2008;452:741–4. 10.1038/nature06776 PubMed DOI
Hecky RE, Kilham P. Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence on the effects of enrichment. Limnol Oceanogr 1988;33:796–822. 10.4319/lo.1988.33.4_part_2.0796 DOI
Rabalais NN. Nitrogen in aquatic ecosystems. Ambio 2002;31:102–12. 10.1579/0044-7447-31.2.102 PubMed DOI
Gomolplitinant KM, Saier MH. Evolution of the oligopeptide transporter family. J Membr Biol 2011;240:89–110. 10.1007/s00232-011-9347-9 PubMed DOI PMC
Béjà O, Aravind L, Koonin EVet al. . Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 2000;289:1902–6. PubMed
Olson DK, Yoshizawa S, Boeuf Det al. . Proteorhodopsin variability and distribution in the North Pacific subtropical gyre. ISME J 2018;12:1047–60. 10.1038/s41396-018-0074-4 PubMed DOI PMC
Keffer JL, Hahn MW, Maresca JA. Characterization of an unconventional rhodopsin from the freshwater actinobacterium Rhodoluna lacicola. J Bacteriol 2015;197:2704–12. 10.1128/JB.00386-15 PubMed DOI PMC
Nakajima Y, Kojima K, Kashiyama Yet al. . Bacterium lacking a known gene for retinal biosynthesis constructs functional rhodopsins. Microbes Environ 2020;35:1–7. 10.1264/jsme2.ME20085 PubMed DOI PMC
Garcia SL, Buck M, Hamilton JJet al. . Model communities hint at promiscuous metabolic linkages between ubiquitous free-living freshwater bacteria. MSphere 2018;3:e00202–18. 10.1128/mSphere.00202-18 PubMed DOI PMC
Kim S, Kang I, Lee JWet al. . Heme auxotrophy in abundant aquatic microbial lineages. Proc Natl Acad Sci USA 2021;118:e2102750118. 10.1073/pnas.2102750118 PubMed DOI PMC
Everse J, Hsia N. The toxicities of native and modified hemoglobins. Free Radic Biol Med 1997;22:1075–99. 10.1016/S0891-5849(96)00499-6 PubMed DOI
Choby JE, Skaar EP. Heme synthesis and acquisition in bacterial pathogens. J Mol Biol 2016;428:3408–28. 10.1016/j.jmb.2016.03.018 PubMed DOI PMC
Castelle CJ, Brown CT, Thomas BCet al. . Unusual respiratory capacity and nitrogen metabolism in a Parcubacterium (OD1) of the candidate phyla radiation. Sci Rep 2017;7:4010. 10.1038/srep40101 PubMed DOI PMC
Ekici S, Pawlik G, Lohmeyer Eet al. . Biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus. Biochim Biophys Acta 2012;1817:898–910. 10.1016/j.bbabio.2011.10.011 PubMed DOI PMC
Han Y, Perner M. The globally widespread genus Sulfurimonas: versatile energy metabolisms and adaptations to redox clines. Front Microbiol 2015;6:989. 10.3389/fmicb.2015.00989 PubMed DOI PMC
Kitzinger K, Padilla CC, Marchant HKet al. . Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. Nat Microbiol 2019;4:234–43. 10.1038/s41564-018-0316-2 PubMed DOI PMC