1887

Abstract

Biocathode communities are of interest for a variety of applications, including electrosynthesis, bioremediation, and biosensors, yet much remains to be understood about the biological processes that occur to enable these communities to grow. One major difficulty in understanding these communities is that the critical autotrophic organisms are difficult to cultivate. An uncultivated, electroautotrophic bacterium previously identified as an uncultivated member of the family appears to be a key organism in an autotrophic biocathode microbial community. Metagenomic, metaproteomic and metatranscriptomic characterization of this community indicates that there is likely a single organism that utilizes electrons from the cathode to fix CO, yet this organism has not been obtained in pure culture. Fluorescence hybridization reveals that the organism grows as rod-shaped cells approximately 1.8 × 0.6 µm, and forms large clumps on the cathode. The genomic DNA G+C content was 59.2 mol%. Here we identify the key features of this organism and propose ‘ Tenderia electrophaga’, within the on the basis of low nucleotide and predicted protein sequence identity to known members of the orders and .

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2016-06-10
2020-01-27
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References

  1. Bose A., Gardel E. J., Vidoudez C., Parra E. A., Girguis P. R.. 2014; Electron uptake by iron-oxidizing phototrophic bacteria. Nat Commun5: [CrossRef][PubMed]
    [Google Scholar]
  2. Childers S. E., Ciufo S., Lovley D. R.. 2002; Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature416:767–769 [CrossRef][PubMed]
    [Google Scholar]
  3. Chin C. S., Alexander D. H., Marks P., Klammer A. A., Drake J., Heiner C., Clum A., Copeland A., Huddleston J., Eichler E. E.. 2013; Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods10:563–569 [CrossRef][PubMed]
    [Google Scholar]
  4. Clark T. A., Murray I. A., Morgan R. D., Kislyuk A. O., Spittle K. E., Boitano M., Fomenkov A., Roberts R. J., Korlach J.. 2012; Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. Nucleic Acids Res40:e29e29 [CrossRef][PubMed]
    [Google Scholar]
  5. Drake S. L., Koomey M.. 1995; The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae . Mol Microbiol18:975–986 [CrossRef][PubMed]
    [Google Scholar]
  6. Emerson D., Floyd M. M.. 2005; Enrichment and isolation of iron-oxidizing bacteria at neutral pH. Methods Enzymol397:112–123 [CrossRef][PubMed]
    [Google Scholar]
  7. Forward J. A., Behrendt M. C., Wyborn N. R., Cross R., Kelly D. J.. 1997; TRAP transporters: A new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse Gram-negative bacteria. J Bacteriol179:5482–5493[PubMed]
    [Google Scholar]
  8. Fuchs B., Pernthaler J., Amann R.. 2007; Single cell identification by fluorescence in situ hybridization. Methods for General and Molecular Microbiology3:886–896
    [Google Scholar]
  9. Higgins C. F.. 2001; ABC transporters: Physiology, structure and mechanism–an overview. Res Microbiol152:205–210 [CrossRef][PubMed]
    [Google Scholar]
  10. Ishii T., Kawaichi S., Nakagawa H., Hashimoto K., Nakamura R.. 2015; From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe (II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources. Front Microbiol6: [CrossRef][PubMed]
    [Google Scholar]
  11. Jeon B. Y., Jung I. L., Park D. H.. 2012; Enrichment and isolation of CO2-fixing bacteria with electrochemical reducing power as a sole energy source. Journal of Environmental Protection3:[CrossRef]
    [Google Scholar]
  12. Karp P. D., Paley S. M., Krummenacker M., Latendresse M., Dale J. M., Lee T. J., Kaipa P., Gilham F., Spaulding A., Popescu L.. 2010; Pathway Tools version 13.0: Integrated software for pathway/genome informatics and systems biology. Brief Bioinform11: [CrossRef][PubMed]
    [Google Scholar]
  13. Kimura M.. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol16:111–120 [CrossRef][PubMed]
    [Google Scholar]
  14. Le S. Q., Gascuel O.. 2008; An improved general amino acid replacement matrix. Mol Biol Evol25:1307–1320 [CrossRef][PubMed]
    [Google Scholar]
  15. Leary D. H., Hervey W. J., Malanoski A. P., Wang Z., Eddie B. J., Tender G. S., Vora G. J., Tender L. M., Lin B., Strycharz-Glaven S. M.. 2015; Metaproteomic evidence of changes in protein expression following a change in electrode potential in a robust biocathode microbiome. Proteomics15:3486–3496 [CrossRef][PubMed]
    [Google Scholar]
  16. Manz W., Amann R., Ludwig W., Wagner M., Schleifer K.-H.. 1992; Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: Problems and solutions. Syst Appl Microbiol15:593–600 [CrossRef]
    [Google Scholar]
  17. Marshall C. W., Ross D. E., Fichot E. B., Norman R. S., May H. D.. 2012; Electrosynthesis of commodity chemicals by an autotrophic microbial community. Appl Environ Microbiol78:8412–8420 [CrossRef][PubMed]
    [Google Scholar]
  18. Martens J. H., Barg H., Warren M. J., Jahn D.. 2002; Microbial production of vitamin B12. Appl Microbiol Biotechnol58:275–285 [CrossRef][PubMed]
    [Google Scholar]
  19. Mattick J. S.. 2002; Type IV pili and twitching motility. Annu Rev Microbiol56:289–314 [CrossRef][PubMed]
    [Google Scholar]
  20. Murray R. G., Stackebrandt E.. 1995; Taxonomic note: Implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol45:186–187 [CrossRef][PubMed]
    [Google Scholar]
  21. Nei M., Kumar S.. 2000; Molecular Evolution and Phylogenetics : Oxford University Press.;
    [Google Scholar]
  22. Overbeek R., Olson R., Pusch G. D., Olsen G. J., Davis J. J., Disz T., Edwards R. A., Gerdes S., Parrello B., Shukla M.. 2014; The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res42:D206–D214 [CrossRef][PubMed]
    [Google Scholar]
  23. PacBio SampleNet– Shared Protocol. 2014; 10 kb to 20 kb template preparation and sequencing with low-input DNA. http://www.pacb.com/wp-content/uploads/2015/09/Shared-282 Protocol-10-kb-to-20-Kb-Template-Preparation-with-Low-Input-DNA.pdf
  24. Parks D. H., Imelfort M., Skennerton C. T., Hugenholtz P., Tyson G. W.. 2015; CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res25:1043–1055 [CrossRef]
    [Google Scholar]
  25. Pruesse E., Peplies J., Glöckner F. O.. 2012; SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics28:1823–1829 [CrossRef][PubMed]
    [Google Scholar]
  26. Rabaey K., Rozendal R. A.. 2010; Microbial electrosynthesis - revisiting the electrical route for microbial production. Nat Rev Microbiol8:706–716 [CrossRef][PubMed]
    [Google Scholar]
  27. Rosenbaum M. A., Franks A. E.. 2014; Microbial catalysis in bioelectrochemical technologies: Status quo, challenges and perspectives. Appl Microbiol Biotechnol98:509–518 [CrossRef][PubMed]
    [Google Scholar]
  28. Rowe A. R., Chellamuthu P., Lam B., Okamoto A., Nealson K. H.. 2014; Marine sediments microbes capable of electrode oxidation as a surrogate for lithotrophic insoluble substrate metabolism. Front Microbiol5:784 [CrossRef][PubMed]
    [Google Scholar]
  29. Schwartz R., Dayhoff M.. 1978; Matrices for detecting distant relationships. Atlas of Protein Sequence and Structure5:353–358
    [Google Scholar]
  30. Silverman M., Simon M.. 1977; Chemotaxis in Escherichia coli: methylation of che gene products. Proc Natl Acad Sci U S A74:3317–3321[PubMed][CrossRef]
    [Google Scholar]
  31. Smith M. A., Finel M., Korolik V., Mendz G. L.. 2000; Characteristics of the aerobic respiratory chains of the microaerophiles Campylobacter jejuni and Helicobacter pylori . Arch Microbiol174:1–10 [CrossRef][PubMed]
    [Google Scholar]
  32. Strycharz-Glaven S. M., Glaven R. H., Wang Z., Zhou J., Vora G. J., Tender L. M.. 2013; Electrochemical investigation of a microbial solar cell reveals a nonphotosynthetic biocathode catalyst. Appl Environ Microbiol79:3933–3942 [CrossRef][PubMed]
    [Google Scholar]
  33. Summers Z. M., Gralnick J. A., Bond D. R.. 2013; Cultivation of an obligate Fe(II)-oxidizing lithoautotrophic bacterium using electrodes. mBio4:e0042000412 [CrossRef][PubMed]
    [Google Scholar]
  34. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S.. 2013; MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  35. Wang Z., Leary D. H., Malanoski A. P., Li R. W., Hervey W. J., Eddie B. J., Tender G. S., Yanosky S. G., Vora G. J., other authors. 2015; A previously uncharacterized, nonphotosynthetic member of the Chromatiaceae is the primary CO2-fixing constituent in a self-regenerating biocathode. Appl Environ Microbiol81:699–712 [CrossRef][PubMed]
    [Google Scholar]
  36. ZoBell C. E.. 1941; Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J Mar Res4:42–75
    [Google Scholar]
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