The candidate phylum Poribacteria by single-cell genomics: New insights into phylogeny, cell-compartmentation, eukaryote-like repeat proteins, and other genomic features

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Kamke, Janine ^a   Rinke, Christian ^b   Schwientek, Patrick ^b   Mavromatis, Kostas ^b   Ivanova, Natalia ^b   Sczyrba, Alexander ^b,c   Woyke, Tanja ^b   Hentschel, Ute ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b DOE JOINT GENOME INSTITUTE   (United States)

^c BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR;

ARTICLE; BACTERIAL GENOME; BACTERIUM; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; GENE SEQUENCE; GENETIC PROCEDURES; LEUCINE RICH REPEAT; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; POPULATION ABUNDANCE; PORIBACTERIA; PROTEIN DOMAIN; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SINGLE CELL GENOMICS; SYMBIONT; TETRATRICOPEPTIDE REPEAT;

ANIMALS; BACTERIA; BACTERIAL PROTEINS; GENETIC VARIATION; GENOME, BACTERIAL; GENOMICS; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SINGLE-CELL ANALYSIS;

EID: 84900313954     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087353     Document Type: Article

References (68)

1. Kamke J, Bayer K, Woyke T, Hentschel U (2012) Exploring symbioses by single-cell genomics. Biol Bull 223: 30-43.
2. Stepanauskas R (2012) Single cell genomics: an individual look at microbes. Curr Opin Microbiol 15: 613-620.
3. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, et al. (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499: 431-437.
4. Kamke J, Sczyrba A, Ivanova N, Schwientek P, Rinke C, et al. (2013) Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges. ISME J 7: 2287-2300.
5. Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum "Poribacteria" in marine sponges. Appl Environ Microb 70: 3724-3732. (Pubitemid 38745923)
6. Pham VD, Konstantinidis KT, Palden T, DeLong EF (2008) Phylogenetic analyses of ribosomal DNA-containing bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific subtropical gyre. Environ Microbiol 10: 2313-2330.
7. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, et al. (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082.
8. Taylor MW, Tsai P, Simister RL, Deines P, Botte E, et al. (2013) "Spongespecific" bacteria are widespread (but rare) in diverse marine environments. ISME J 7: 438-443.
9. Lafi FF, Fuerst JA, Fieseler L, Engels C, Goh WWL, et al. (2009) Widespread distribution of Poribacteria in Demospongiae. Appl Environ Microb 75: 5695-5699.
10. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, et al. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6: 564-576.
11. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiol Mol Biol R 71: 295-347. (Pubitemid 46954308)
12. Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microb 74: 7694-7708.
13. Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotech 17: 241-249. (Pubitemid 43850263)
14. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, et al. (2011) Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5: 61-70.
15. Markowitz VM, Kyrpides NC (2007) Comparative genome analysis in the integrated microbial genomes (IMG) system. Methods Mol Biol 395: 35-56. (Pubitemid 350183287)
16. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
17. Quast C, Pruesse E, Yilmaz P, Gerken J (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
18. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: A software environment for sequence data. Nucleic Acids Res 32: 1363-1371. (Pubitemid 38854737)
19. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
20. Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
21. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
22. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37.
23. Price MN, Dehal PS, Arkin AP (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490. doi:10.1371/journal.pone.0009490.
24. Stamatakis A, Aberer AJ, Goll C, Smith SA, Berger SA, et al. (2012) RAxML-Light: a tool for computing terabyte phylogenies. Bioinformatics 28: 2064-2066.
25. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, et al. (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462: 1056-1060.
26. Gupta RS, Bhandari V, Naushad HS (2012) Molecular signatures for the PVC clade (Planctomycetes, Verrucomicrobia, Chlamydiae, and Lentisphaerae) of bacteria provide insights into their evolutionary relationships. Front Microbio 3. doi: 10.3389/fmicb.2012.00327.
27. Lang J, Lang J, Lang J, Darling A, Darling A, et al. (2013) Phylogeny of bacterial and archaeal genomes using conserved genes: supertrees and supermatrices. PLoS ONE 8: e62510. doi:10.1371/journal.pone.0062510.
28. Lagkouvardos I, Jehl MA, Rattei T, Horn M (2013) The signature protein of the PVC superphylum. Appl Environ Microbiol published ahead of print. doi:10.1128/AEM.02655-13.
29. Fuerst JA (2005) Intracellular compartmentation in planctomycetes. Annu RevMicrobiol 59: 299-328.
30. Fuerst JA, Webb RI (1991) Membrane-bounded nucleoid in the eubacterium Gemmatata obscuriglobus. Proc Natl Acad Sci USA 88: 8184-8. (Pubitemid 21915321)
31. Santarella-Mellwig R, Franke J, Jaedicke A, Gorjanacz M, Bauer U, et al. (2010) The compartmentalized bacteria of the Planctomycetes-Verrucomicrobia- Chlamydiae superphylum have membrane coat-like proteins. Plos Biol 8: e1000281. doi:10.1371/journal.pbio.1000281.t002.
32. Santarella-Mellwig R, Pruggnaller S, Roos N, Mattaj IW, Devos DP (2013) Three-dimensional reconstruction of bacteria with a complex endomembrane system. Plos Biol 11: e1001565. doi:10.1371/journal.pbio.1001565.s014.
33. Kerfeld CA, Heinhorst S, Cannon GC (2010) Bacterial Microcompartments. Annu Rev Microbiol 64: 391-408.
34. Yeates TO, Crowley CS, Tanaka S (2010) Bacterial microcompartment organelles: protein shell structure and evolution. Annu Rev Biophys 39: 185-205.
35. Yeates TO, Thompson MC, Bobik TA (2011) The protein shells of bacterial microcompartment organelles. Curr Opin Struc Biol 21: 223-231.
36. Jorda J, Lopez D, Wheatley NM, Yeates TO (2013) Using comparative genomics to uncover new kinds of protein-based metabolic organelles in bacteria. Protein Sci 22: 179-195.
37. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, et al. (2010) Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4: 1557-11567.
38. Siegl A, Hentschel U (2009) PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ Microbiol Rep 2: 507-513.
39. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, et al. (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci USA 109: E1878-E1887.
40. Mittl PR, Schneider-Brachert W (2007) Sel1-like repeat proteins in signal transduction. Cell Signal 19: 20-31. (Pubitemid 44880252)
41. Hussain MM, Strickland DK, Bakillah A (1999) The mammalian low-density lipoprotein receptor family. Annu Rev Nutr 19: 141-172. (Pubitemid 29380600)
42. Davis CG, Goldstein JL, Südhof TC, Anderson RG, Russell DW, et al. (1987) Acid-dependent ligand dissociation and recycling of LDL receptor mediated by growth factor homology region. Nature 326: 760-765. (Pubitemid 17057795)
43. Sato K, Naito M, Yukitake H, Hirakawa H, Shoji M, et al. (2010) A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc Natl Acad Sci USA 107: 276-281.
44. Suen G, Weimer PJ, Stevenson DM, Aylward FO, Boyum J, et al. (2011) The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS ONE 6: e18814. doi:10.1371/journal.pone.0018814.
45. Nguyen KA, Travis J, Potempa J (2007) Does the importance of the C-terminal residues in the maturation of RgpB from Porphyromonas gingivalis reveal a novel mechanism for protein export in a subgroup of gram-negative bacteria? J Bacteriol 189: 833-843. (Pubitemid 46183857)
46. Liu MY, Kjelleberg S, Thomas T (2010) Functional genomic analysis of an uncultured delta-proteobacterium in the sponge Cymbastela concentrica. ISME J 5: 427-435.
47. Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Micro 10: 641-654.
48. Nguyen MTHD, Liu M, Thomas T (2013) Ankyrin-repeat proteins from sponge symbionts modulate amoebal phagocytosis. Mol Ecol. In press. doi:10.1111/mec.12384.
49. Viboud GI, Bliska JB (2005) Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59: 69-89. (Pubitemid 41507424)
50. Bierne H, Cossart P (2002) InlB, a surface protein of Listeria monocytogenes that behaves as an invasin and a growth factor. J Cell Sci.115: 3357-67. (Pubitemid 34994027)
51. Cerveny L, Straskova A, Dankova V, Hartlova A, Ceckova M, et al. (2013) Tetratricopeptide repeat motifs in the world of bacterial pathogens: Role in virulence mechanisms. Infect Immun 81: 629-635.
52. Schwarz-Linek U, Werner JM, Pickford AR (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423: 177-181. (Pubitemid 36569541)
53. Schwarz-Linek U, Höök M, Potts JR (2004) The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol Microbiol 52: 631-641. (Pubitemid 38621735)
54. Kataeva IA, Seidel RD, Shah A, West LT, Li XL, et al. (2002) The fibronectin type 3-like repeat from the Clostridium thermocellum cellobiohydrolase CbhA promotes hydrolysis of cellulose by modifying its surface. Appl Environ Microb 68: 4292-4300. (Pubitemid 34988108)
55. Schofield CJ, McDonough MA (2007) Structural and mechanistic studies on the peroxisomal oxygenase phytanoyl-CoA 2-hydroxylase (PhyH). Biochem Soc Trans 35: 870-875. (Pubitemid 350206385)
56. Hao Y, Winans SC, Glick BR, Charles TC (2010) Identification and characterization of new LuxR/LuxI-type quorum sensing systems from metagenomic libraries. Environ Microbiol 12: 105-117.
57. Reuter K, Pittelkow M, Bursy J, Heine A, Craan T, et al. (2010) Synthesis of 5-hydroxyectoine from ectoine: Crystal structure of the non-heme Iron(II) and 2-oxoglutarate-dependent dioxygenase EctD. PLoS ONE 5: e10647. doi:10.1371/journal.pone.0010647.
58. White AK, Metcalf WW (2007) Microbial metabolism of reduced phosphorus compounds. Annu Rev Microbiol 61: 379-400. (Pubitemid 350058214)
59. Martinez A, Tyson GW, DeLong EF (2010) Widespread known and novel phosphonate utilization pathways in marine bacteria revealed by functional screening and metagenomic analyses. Environ Microbiol 12: 222-238.
60. Fieseler L, Quaiser A, Schleper C, Hentschel U (2006) Analysis of the first genome fragment from the marine sponge-associated, novel candidate phylum Poribacteria by environmental genomics. Environ Microbiol 8: 612-624. (Pubitemid 43363318)
61. Kolowith LC, Ingall ED, Benner R (2001) Composition and cycling of marine organic phosphorus. Limnol Oceanogr 46: 309-320. (Pubitemid 32281607)
62. Clark LL, Ingall ED, Benner R (1999) Marine organic phosphorus cycling: novel insights from nuclear magnetic resonance. Am J Sci 299: 724-737.
63. Villarreal-Chiu JF, Quinn JP, McGrath JW (2012) The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment. Front Microbio 3. doi: 10.3389/fmicb.2012.00019.
64. Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, et al. (2006) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439: 68-71. (Pubitemid 43053629)
65. Mukhamedova KS, Glushenkova AI (2000) Natural Phosphonolipids. Chemistry of Natural Compounds 36: 329-341. (Pubitemid 33254897)
66. Dembitsky VM, Rezanka T, Srebnik M (2003) Lipid compounds of freshwater sponges: family Spongillidae, class Demospongiae. Chemistry and Physics of Lipids 123: 117-155. (Pubitemid 36419527)
67. Dembitskii VM (1988) Lipids of marine origin. IV. 1,2-Di-O- alkylglyceropho-spho- and -phosphonolipids from the marine sponge Ectyodoryx kovdaicum. Chem Nat Compd 24: 642-643.
68. Dyhrman ST, Benitez-Nelson CR, Orchard ED, Haley ST, Pellechia PJ (2009) A microbial source of phosphonates in oligotrophic marine systems. Nature Geosci 2: 696-699.