Targeted isolation and cultivation of uncultivated bacteria by reverse genomics

Cross, Karissa L.; Campbell, James H.; Balachandran, Manasi; Campbell, Alisha G.; Cooper, Sarah J.; Griffen, Ann; Heaton, Matthew; Joshi, Snehal; Klingeman, Dawn; Leys, Eugene; Yang, Zamin; Parks, Jerry M.; Podar, Mircea

doi:10.1038/s41587-019-0260-6

Title: Targeted isolation and cultivation of uncultivated bacteria by reverse genomics

Journal Article · 30 September 2019 · Nature Biotechnology

DOI: https://doi.org/10.1038/s41587-019-0260-6 · OSTI ID:1570133

Cross, Karissa L. ^[1]; Campbell, James H. ^[2]; Balachandran, Manasi ^[3]; Campbell, Alisha G. ^[2]; Cooper, Sarah J. ^[1]; Griffen, Ann ^[4]; Heaton, Matthew ^[5];

^[3];

^[3]; Leys, Eugene ^[4]; Yang, Zamin ^[3];

^[1];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Northwest Missouri State Univ., Maryville, MO (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
The Ohio State Univ., Columbus, OH (United States)
Knoxville Periodontics, Knoxville, TN (United States)

The majority of microorganisms from all taxonomic levels are uncultured. Single-cell genomes and metagenomes continue to increase the known diversity of Bacteria and Archaea; however, while ’omics can be used to infer physiological or ecological roles for species in a community, most of these hypothetical roles remain unvalidated. Here, we report a technique to capture specific microorganisms from complex communities into pure cultures using genome-informed antibody engineering. We apply our reverse genomics approach to isolate and sequence single cells and to cultivate three different species-level lineages of human oral Saccharibacteria (TM7). Using our pure cultures, we show that all three Saccharibacteria species are epibionts of diverse Actinobacteria. We also isolate and cultivate human oral SR1 bacteria, which are members of a lineage of previously uncultured bacteria. Reverse-genomics-enabled cultivation of microorganisms can be applied to any species from any environment and has the potential to unlock the isolation, cultivation and characterization of species from as-yet-uncultured branches of the microbial tree of life.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: National Institute of Health (NIH); National Science Foundation (NSF); USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1570133

Journal Information:: Nature Biotechnology, Journal Name: Nature Biotechnology Journal Issue: 11 Vol. 37; ISSN 1087-0156

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (94)

Improved recognition of native-like protein structures using a combination of sequence-dependent and sequence-independent features of proteins Simons, Kim T.; Ruczinski, Ingo; Kooperberg, Charles Proteins: Structure, Function, and Genetics, Vol. 34, Issue 1 https://doi.org/10.1002/(SICI)1097-0134(19990101)34:1<82::AID-PROT7>3.0.CO;2-A	journal	January 1999
Prediction of continuous B-cell epitopes in an antigen using recurrent neural network Saha, Sudipto; Raghava, G. P. S. Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 1 https://doi.org/10.1002/prot.21078	journal	August 2006
Learning generative models for protein fold families Balakrishnan, Sivaraman; Kamisetty, Hetunandan; Carbonell, Jaime G. Proteins: Structure, Function, and Bioinformatics, Vol. 79, Issue 4 https://doi.org/10.1002/prot.22934	journal	January 2011
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Protein Data Bank (PDB): The Single Global Macromolecular Structure Archive Burley, Stephen K.; Berman, Helen M.; Kleywegt, Gerard J. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-7000-1_26	book	January 2017
Complex Evolution of the Mismatch Repair System in Eukaryotes is Illuminated by Novel Archaeal Genomes Hofstatter, Paulo G.; Lahr, Daniel J. G. Journal of Molecular Evolution, Vol. 89, Issue 1-2 https://doi.org/10.1007/s00239-020-09979-5	journal	January 2021
Phenotypic and Physiological Characterization of the Epibiotic Interaction Between TM7x and Its Basibiont Actinomyces Bor, Batbileg; Poweleit, Nicole; Bois, Justin S. Microbial Ecology, Vol. 71, Issue 1 https://doi.org/10.1007/s00248-015-0711-7	journal	November 2015
A comparison of human dental plaque microcosm biofilms grown in an undefined medium and a chemically defined artificial saliva Wong, L.; Sissions, C. H. Archives of Oral Biology, Vol. 46, Issue 6 https://doi.org/10.1016/S0003-9969(01)00016-4	journal	June 2001
Siderophores from Neighboring Organisms Promote the Growth of Uncultured Bacteria D'Onofrio, Anthony; Crawford, Jason M.; Stewart, Eric J. Chemistry & Biology, Vol. 17, Issue 3 https://doi.org/10.1016/j.chembiol.2010.02.010	journal	March 2010
Novel Microbial Diversity and Functional Potential in the Marine Mammal Oral Microbiome Dudek, Natasha K.; Sun, Christine L.; Burstein, David Current Biology, Vol. 27, Issue 24 https://doi.org/10.1016/j.cub.2017.10.040	journal	December 2017
The phenomenon of microbial uncultivability Epstein, Ss Current Opinion in Microbiology, Vol. 16, Issue 5 https://doi.org/10.1016/j.mib.2013.08.003	journal	October 2013
A novel recombinant vaccine candidate comprising PBP2a and autolysin against Methicillin Resistant Staphylococcus aureus confers protection in the experimental mice Haghighat, Setareh; Siadat, Seyed Davar; Sorkhabadi, Seyed Mehdi Rezayat Molecular Immunology, Vol. 91 https://doi.org/10.1016/j.molimm.2017.08.013	journal	November 2017
A new symbiotic nanoarchaeote (Candidatus Nanoclepta minutus) and its host (Zestosphaera tikiterensis gen. nov., sp. nov.) from a New Zealand hot spring St. John, Emily; Liu, Yitai; Podar, Mircea Systematic and Applied Microbiology, Vol. 42, Issue 1 https://doi.org/10.1016/j.syapm.2018.08.005	journal	January 2019
Sequence-structure relationships in polysaccharide co-polymerase (PCP) proteins Morona, Renato; Purins, Leanne; Tocilj, Ante Trends in Biochemical Sciences, Vol. 34, Issue 2 https://doi.org/10.1016/j.tibs.2008.11.001	journal	February 2009
The feline oral microbiome: A provisional 16S rRNA gene based taxonomy with full-length reference sequences Dewhirst, Floyd E.; Klein, Erin A.; Bennett, Marie-Louise Veterinary Microbiology, Vol. 175, Issue 2-4 https://doi.org/10.1016/j.vetmic.2014.11.019	journal	February 2015
Distinctive Attributes of β-Lactam Target Proteins in Acinetobacter baumannii Relevant to Development of New Antibiotics Han, Seungil; Caspers, Nicole; Zaniewski, Richard P. Journal of the American Chemical Society, Vol. 133, Issue 50 https://doi.org/10.1021/ja208835z	journal	December 2011
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont Huber, Harald; Hohn, Michael J.; Rachel, Reinhard Nature, Vol. 417, Issue 6884 https://doi.org/10.1038/417063a	journal	May 2002
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation Browne, Hilary P.; Forster, Samuel C.; Anonye, Blessing O. Nature, Vol. 533, Issue 7604 https://doi.org/10.1038/nature17645	journal	May 2016
Asgard archaea illuminate the origin of eukaryotic cellular complexity Zaremba-Niedzwiedzka, Katarzyna; Caceres, Eva F.; Saw, Jimmy H. Nature, Vol. 541, Issue 7637 https://doi.org/10.1038/nature21031	journal	January 2017
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam Nature Biotechnology, Vol. 31, Issue 6 https://doi.org/10.1038/nbt.2579	journal	May 2013
Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment Wurch, Louie; Giannone, Richard J.; Belisle, Bernard S. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12115	journal	July 2016
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Harnessing the landscape of microbial culture media to predict new organism–media pairings Oberhardt, Matthew A.; Zarecki, Raphy; Gronow, Sabine Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9493	journal	October 2015
HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment Remmert, Michael; Biegert, Andreas; Hauser, Andreas Nature Methods, Vol. 9, Issue 2 https://doi.org/10.1038/nmeth.1818	journal	December 2011
Practical innovations for high-throughput amplicon sequencing Lundberg, Derek S.; Yourstone, Scott; Mieczkowski, Piotr Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2634	journal	September 2013
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Culture of previously uncultured members of the human gut microbiota by culturomics Lagier, Jean-Christophe; Khelaifia, Saber; Alou, Maryam Tidjani Nature Microbiology, Vol. 1, Issue 12 https://doi.org/10.1038/nmicrobiol.2016.203	journal	November 2016
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics Rinke, Christian; Lee, Janey; Nath, Nandita Nature Protocols, Vol. 9, Issue 5 https://doi.org/10.1038/nprot.2014.067	journal	April 2014
In situ cultivation of previously uncultivable microorganisms using the ichip Berdy, Brittany; Spoering, Amy L.; Ling, Losee L. Nature Protocols, Vol. 12, Issue 10 https://doi.org/10.1038/nprot.2017.074	journal	September 2017
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria Nature Microbiology, Vol. 2, Issue 11 https://doi.org/10.1038/s41564-017-0012-7	journal	September 2017
GABA-modulating bacteria of the human gut microbiota Strandwitz, Philip; Kim, Ki Hyun; Terekhova, Darya Nature Microbiology, Vol. 4, Issue 3 https://doi.org/10.1038/s41564-018-0307-3	journal	December 2018
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik Nature Reviews Microbiology, Vol. 16, Issue 10 https://doi.org/10.1038/s41579-018-0076-2	journal	September 2018
Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis Yuan, Y.; Barrett, D.; Zhang, Y. Proceedings of the National Academy of Sciences, Vol. 104, Issue 13 https://doi.org/10.1073/pnas.0701160104	journal	March 2007
Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth Marcy, Y.; Ouverney, C.; Bik, E. M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 29, p. 11889-11894 https://doi.org/10.1073/pnas.0704662104	journal	July 2007
Crystal structure of the membrane-bound bifunctional transglycosylase PBP1b from Escherichia coli Sung, M. -T.; Lai, Y. -T.; Huang, C. -Y. Proceedings of the National Academy of Sciences, Vol. 106, Issue 22 https://doi.org/10.1073/pnas.0904030106	journal	May 2009
Crystal structure of Staphylococcus aureus transglycosylase in complex with a lipid II analog and elucidation of peptidoglycan synthesis mechanism Huang, C. -Y.; Shih, H. -W.; Lin, L. -Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 17 https://doi.org/10.1073/pnas.1203900109	journal	April 2012
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota Campbell, J. H.; O'Donoghue, P.; Campbell, A. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545 https://doi.org/10.1073/pnas.1303090110	journal	March 2013
Assessing the utility of coevolution-based residue-residue contact predictions in a sequence- and structure-rich era Kamisetty, H.; Ovchinnikov, S.; Baker, D. Proceedings of the National Academy of Sciences, Vol. 110, Issue 39 https://doi.org/10.1073/pnas.1314045110	journal	September 2013
Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle He, Xuesong; McLean, Jeffrey S.; Edlund, Anna Proceedings of the National Academy of Sciences, Vol. 112, Issue 1 https://doi.org/10.1073/pnas.1419038112	journal	December 2014
Biogeography of a human oral microbiome at the micron scale Mark Welch, Jessica L.; Rossetti, Blair J.; Rieken, Christopher W. Proceedings of the National Academy of Sciences, Vol. 113, Issue 6 https://doi.org/10.1073/pnas.1522149113	journal	January 2016
Microfluidic droplet platform for ultrahigh-throughput single-cell screening of biodiversity Terekhov, Stanislav S.; Smirnov, Ivan V.; Stepanova, Anastasiya V. Proceedings of the National Academy of Sciences, Vol. 114, Issue 10 https://doi.org/10.1073/pnas.1621226114	journal	February 2017
Nonlinear partial differential equations and applications: Cultivating the uncultured Zengler, K.; Toledo, G.; Rappe, M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 24 https://doi.org/10.1073/pnas.252630999	journal	November 2002
Streptococcus agalactiae Capsule Polymer Length and Attachment Is Determined by the Proteins CpsABCD Toniolo, Chiara; Balducci, Evita; Romano, Maria Rosaria Journal of Biological Chemistry, Vol. 290, Issue 15 https://doi.org/10.1074/jbc.M114.631499	journal	February 2015
The multi-omics promise in context: from sequence to microbial isolate Gutleben, Johanna; Chaib De Mares, Maryam; van Elsas, Jan Dirk Critical Reviews in Microbiology, Vol. 44, Issue 2 https://doi.org/10.1080/1040841X.2017.1332003	journal	May 2017
Environmental Diversity of Bacteria and Archaea DeLong, Edward F.; Pace, Norman R. Systematic Biology, Vol. 50, Issue 4 https://doi.org/10.1080/10635150118513	journal	August 2001
Environmental Diversity of Bacteria and Archaea DeLong, Edward F.; Pace, Norman R. Systematic Biology, Vol. 50, Issue 4 https://doi.org/10.1080/106351501750435040	journal	August 2001
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Immunogenicity of meningococcal PBP2 during natural infection and protective activity of anti-PBP2 antibodies against meningococcal bacteraemia in mice Zarantonelli, Maria Leticia; Antignac, Aude; Lancellotti, Marcelo Journal of Antimicrobial Chemotherapy, Vol. 57, Issue 5 https://doi.org/10.1093/jac/dkl066	journal	March 2006
The integrated microbial genomes (IMG) system Markowitz, V. M. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj024	journal	January 2006
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences Huerta-Cepas, Jaime; Szklarczyk, Damian; Forslund, Kristoffer Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1248	journal	November 2015
Intestinal TM7 bacterial phylogenies in active inflammatory bowel disease Kuehbacher, T.; Rehman, A.; Lepage, P. Journal of Medical Microbiology, Vol. 57, Issue 12 https://doi.org/10.1099/jmm.0.47719-0	journal	December 2008
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Diversity and genomic insights into the uncultured C hloroflexi from the human microbiota : Uncultured human-associated Campbell, Alisha G.; Schwientek, Patrick; Vishnivetskaya, Tatiana Environmental Microbiology, Vol. 16, Issue 9 https://doi.org/10.1111/1462-2920.12461	journal	April 2014
Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages: N- and C-cycling organisms in the subsurface Hug, Laura A.; Thomas, Brian C.; Sharon, Itai Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12930	journal	July 2015
The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis Sauvage, Eric; Kerff, Frédéric; Terrak, Mohammed FEMS Microbiology Reviews, Vol. 32, Issue 2 https://doi.org/10.1111/j.1574-6976.2008.00105.x	journal	March 2008
The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis Sauvage, Eric; Kerff, Frédéric; Terrak, Mohammed FEMS Microbiology Reviews, Vol. 32, Issue 3 https://doi.org/10.1111/j.1574-6976.2008.00115.x	journal	May 2008
Recent findings on the viable but nonculturable state in pathogenic bacteria Oliver, James D. FEMS Microbiology Reviews, Vol. 34, Issue 4 https://doi.org/10.1111/j.1574-6976.2009.00200.x	journal	July 2010
Structural Insight into the Transglycosylation Step of Bacterial Cell-Wall Biosynthesis Lovering, A. L.; de Castro, L. H.; Lim, D. Science, Vol. 315, Issue 5817 https://doi.org/10.1126/science.1136611	journal	March 2007
Protein structure determination using metagenome sequence data Ovchinnikov, Sergey; Park, Hahnbeom; Varghese, Neha Science, Vol. 355, Issue 6322 https://doi.org/10.1126/science.aah4043	journal	January 2017
Interbacterial Adhesion Networks within Early Oral Biofilms of Single Human Hosts Palmer, Robert J.; Shah, Nehal; Valm, Alex Applied and Environmental Microbiology, Vol. 83, Issue 11 https://doi.org/10.1128/AEM.00407-17	journal	March 2017
Axenic Culture of a Candidate Division TM7 Bacterium from the Human Oral Cavity and Biofilm Interactions with Other Oral Bacteria Soro, Valeria; Dutton, Lindsay C.; Sprague, Susan V. Applied and Environmental Microbiology, Vol. 80, Issue 20 https://doi.org/10.1128/AEM.01827-14	journal	August 2014
Targeted Access to the Genomes of Low-Abundance Organisms in Complex Microbial Communities Podar, M.; Abulencia, C. B.; Walcher, M. Applied and Environmental Microbiology, Vol. 73, Issue 10 https://doi.org/10.1128/AEM.02985-06	journal	March 2007
New Approaches for Isolation of Previously Uncultivated Oral Bacteria Sizova, M. V.; Hohmann, T.; Hazen, A. Applied and Environmental Microbiology, Vol. 78, Issue 1 https://doi.org/10.1128/AEM.06813-11	journal	November 2011
Prevalence of Bacteria of Division TM7 in Human Subgingival Plaque and Their Association with Disease Brinig, M. M.; Lepp, P. W.; Ouverney, C. C. Applied and Environmental Microbiology, Vol. 69, Issue 3 https://doi.org/10.1128/AEM.69.3.1687-1694.2003	journal	March 2003
Microcolony Cultivation on a Soil Substrate Membrane System Selects for Previously Uncultured Soil Bacteria Ferrari, B. C.; Binnerup, S. J.; Gillings, M. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8714-8720.2005	journal	December 2005
Identification of Streptococcus pneumoniae Cps2C Residues That Affect Capsular Polysaccharide Polymerization, Cell Wall Ligation, and Cps2D Phosphorylation Byrne, J. P.; Morona, J. K.; Paton, J. C. Journal of Bacteriology, Vol. 193, Issue 9 https://doi.org/10.1128/JB.00074-11	journal	March 2011
The Human Oral Microbiome Dewhirst, F. E.; Chen, T.; Izard, J. Journal of Bacteriology, Vol. 192, Issue 19 https://doi.org/10.1128/JB.00542-10	journal	July 2010
Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity Hugenholtz, Philip; Goebel, Brett M.; Pace, Norman R. Journal of Bacteriology, Vol. 180, Issue 18 https://doi.org/10.1128/JB.180.18.4765-4774.1998	journal	September 1998
Molecular Detection of Cellulosimicrobium cellulans as the Etiological Agent of a Chronic Tongue Ulcer in a Human Immunodeficiency Virus-Positive Patient Heym, B.; Gehanno, P.; Friocourt, V. Journal of Clinical Microbiology, Vol. 43, Issue 8 https://doi.org/10.1128/JCM.43.8.4269-4271.2005	journal	August 2005
Insights into the Evolution of Host Association through the Isolation and Characterization of a Novel Human Periodontal Pathobiont, Desulfobulbus oralis Cross, Karissa L.; Chirania, Payal; Xiong, Weili mBio, Vol. 9, Issue 2 https://doi.org/10.1128/mBio.02061-17	journal	March 2018
Draft Genome Sequence of Comamonas aquatilis Strain LK (= CSUR P6418 = CECT 9772), Isolated from the Planarian Schmidtea mediterranea Kangale, Luis Johnson; Levasseur, Anthony; Raoult, Didier Microbiology Resource Announcements, Vol. 10, Issue 5 https://doi.org/10.1128/mra.00297-20	journal	February 2021
Present and Future of Culturing Bacteria Overmann, Jörg; Abt, Birte; Sikorski, Johannes Annual Review of Microbiology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-micro-090816-093449	journal	September 2017
Hidden Markov model speed heuristic and iterative HMM search procedure Johnson, L. Steven; Eddy, Sean R.; Portugaly, Elon BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-431	journal	August 2010
Establishment and metabolic analysis of a model microbial community for understanding trophic and electron accepting interactions of subsurface anaerobic environments Miller, Lance D.; Mosher, Jennifer J.; Venkateswaran, Amudhan BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-149	journal	January 2010
Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park Podar, Mircea; Makarova, Kira S.; Graham, David E. Biology Direct, Vol. 8, Issue 1 https://doi.org/10.1186/1745-6150-8-9	journal	April 2013
Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis Vu, Nga T. T.; Zenger, Kyall R.; Guppy, Jarrod L. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-07084-x	journal	September 2020
Generalized Fragment Picking in Rosetta: Design, Protocols and Applications Gront, Dominik; Kulp, Daniel W.; Vernon, Robert M. PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0023294	journal	August 2011
The Canine Oral Microbiome Dewhirst, Floyd E.; Klein, Erin A.; Thompson, Emily C. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0036067	journal	April 2012
Multiple Single-Cell Genomes Provide Insight into Functions of Uncultured Deltaproteobacteria in the Human Oral Cavity Campbell, Alisha G.; Campbell, James H.; Schwientek, Patrick PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0059361	journal	March 2013
In Vitro Cultivation of ‘Unculturable’ Oral Bacteria, Facilitated by Community Culture and Media Supplementation with Siderophores Vartoukian, Sonia R.; Adamowska, Aleksandra; Lawlor, Megan PLOS ONE, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pone.0146926	journal	January 2016
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans Heimerl, Thomas; Flechsler, Jennifer; Pickl, Carolin Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01072	journal	June 2017
Isolation of Uncultured Bacteria from Antarctica Using Long Incubation Periods and Low Nutritional Media Pulschen, Andre A.; Bendia, Amanda G.; Fricker, Ashwana D. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01346	journal	July 2017
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences Jaime, Huerta-Cepas,; Damian, Szklarczyk,; Kristoffer, Forslund, Oxford University Press https://doi.org/10.5167/uzh-120037	text	January 2016
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
Linking pangenomes and metagenomes: the Prochlorococcus metapangenome Delmont, Tom O.; Eren, A. Murat PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4320	journal	January 2018

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Additional file 1 of Genomic representativeness and chimerism in large collections of SAGs and MAGs of marine prokaryoplankton Chang, Tianyi; Gavelis, Gregory S.; Brown, Julia M. figshare https://doi.org/10.6084/m9.figshare.26309024.v1	image	January 2024
Next-generation physiology approaches to study microbiome function at single cell level Hatzenpichler, Roland; Krukenberg, Viola; Spietz, Rachel L. Nature Reviews Microbiology, Vol. 18, Issue 4 https://doi.org/10.1038/s41579-020-0323-1	journal	February 2020
Culturing the uncultured Lewis, William H.; Ettema, Thijs J. G. Nature Biotechnology, Vol. 37, Issue 11 https://doi.org/10.1038/s41587-019-0300-2	journal	October 2019
Genome‐inferred spatio‐temporal resolution of an uncultivated Roizmanbacterium reveals its ecological preferences in groundwater Geesink, Patricia; Wegner, Carl‐Eric; Probst, Alexander J. Environmental Microbiology, Vol. 22, Issue 2 https://doi.org/10.1111/1462-2920.14865	journal	December 2019
Methane oxidation and methylotroph population dynamics in groundwater mesocosms Kuloyo, Olukayode; Ruff, S. Emil; Cahill, Aaron Environmental Microbiology, Vol. 22, Issue 4 https://doi.org/10.1111/1462-2920.14929	journal	April 2020
Insights Obtained by Culturing Saccharibacteria With Their Bacterial Hosts Bor, B.; Collins, A. J.; Murugkar, P. P. Journal of Dental Research, Vol. 99, Issue 6 https://doi.org/10.1177/0022034520905792	journal	February 2020

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