Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges

ISME Journal

Volumn 5, Issue 1, 2011, Pages 61-70

  Siegl, Alexander ^a,e   Kamke, Janine ^a   Hochmuth, Thomas ^b   Piel, Jörn ^b   Richter, Michael ^c   Liang, Chunguang ^d   Dandekar, Thomas ^d   Hentschel, Ute ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c RIBOCON GMBH   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e UNIVERSITY OF VIENNA   (Austria)

Author keywords

marine; Poribacteria; single cell genomics; sponge; symbiosis

Indexed keywords

POLYKETIDE SYNTHASE; STEROL;

BACTERIUM; BIOMARKER; CARBON DIOXIDE; CELL ORGANELLE; ENZYME ACTIVITY; FLUORESCENCE; GENE EXPRESSION; GENOME; GENOMICS; MARINE ENVIRONMENT; PEPTIDE; POLYMERASE CHAIN REACTION; PROTEIN; SPONGE; SYMBIOSIS;

ANIMAL; ARTICLE; BACTERIAL GENOME; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIOSYNTHESIS; CLASSIFICATION; GENETICS; GENOMICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; SPONGE (PORIFERA); SYMBIOSIS;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYKETIDE SYNTHASES; PORIFERA; STEROLS; SYMBIOSIS;

MEDITERRANEAN SEA;

APLYSINA AEROPHOBA; BACTERIA (MICROORGANISMS); CANDIDATUS PORIBACTERIA; METAZOA; NEGIBACTERIA;

EID: 78650591665     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2010.95     Document Type: Article

References (54)

1. Bayer K, Schmitt S, Hentschel U. (2008). Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environ Microbiol 10: 2942-2955.
2. Bergquist PR, Hofheinz W, Oesterhelt G. (1980). Sterol composition and the classification of the Demospongiae. Biochem System Ecol 8: 423-435.
3. Binga EK, Lasken RS, Neufeld JD. (2008). Something from (almost) nothing: the impact of multiple displacement amplification on microbial ecology. ISME J 2: 233-241.
4. Bode HB, Zeggel B, Silakowski B, Wenzel SC, Reichenbach H, Müller R. (2003). Steroid biosynthesis in prokaryotes: identification of myxobacterial steroids and cloning of the first bacterial 2,3(S)-oxidosqualene cyclase from the myxobacterium Stigmatella aurantiaca. Mol Microbiol 47: 471-481.
5. Dean FB, Hosono S, Fang L,Wu X, Faruqi AF, Bray-Ward P et al. (2002). Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci USA 99: 5261-5266.
6. Dean FB, Nelson JR, Giesler TL, Lasken RS. (2001). Rapid amplification of plasmid and phage DNA using Phi 29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res 11: 1095-1099.
7. Drake HL, Daniel SL. (2004). Physiology of the thermophilic acetogen Moorella thermoacetica. Res Microbiol 155: 869-883.
8. Fieseler L, Hentschel U, Grozdanov L, Schirmer A, Wen G, Platzer M et al. (2007). Widespread occurrence and genomic context of unusually small polyketide synthase genes in microbial consortia associated with marine sponges. Appl Environ Microbiol 73: 2144-2155.
9. Fieseler L, Horn M, Wagner M, Hentschel U. (2004). Discovery of the novel candidate phylum 'Poribacteria' in marine sponges. Appl Environ Microbiol 70: 3724-3732.
10. 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.
11. Fuerst JA, Webb RI, Garson MJ, Hardy L, Reiswig HM. (1999). Membrane-bounded nuclear bodies in a diverse range of microbial symbionts of Great Barrier Reef sponges. Mem Queensland Mus 44: 193-203.
12. Glöckner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig Wet al. (2003). Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100: 8298-8303.
13. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM et al. (2006a). Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4: e95.
14. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, Sugahara J et al. (2006b). Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci USA 103: 18296-18301.
15. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J et al. (2002). Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68: 4431-4440.
16. Hoffmann F, Roy H, Bayer K, Hentschel U, Pfannkuchen M, Brümmer F et al. (2008). Oxygen dynamics and transport in the Mediterranean sponge Aplysina aerophoba. Mar Biol 153: 1257-1264.
17. Hutchison III CA, Venter JC. (2006). Single-cell genomics. Nat Biotechnol 24: 657-658.
18. Ishoey T, Woyke T, Stepanauskas R, Novotny M, Lasken RS. (2008). Genomic sequencing of single microbial cells from environmental samples. Curr Opin Microbiol 11: 198-204.
19. Kodner RB, Summons RE, Pearson A, King N, Knoll AH. (2008). Sterols in a unicellular relative of the metazoans. Proc Natl Acad Sci USA 105: 9897-9902.
20. Lafi FF, Fuerst JA, Fieseler L, Hentschel U. (2009). Widespread distribution of poribacteria in Demospongiae. Appl Environ Microbiol 75: 5695-5699.
21. Lamb DC, Jackson CJ, Warrilow AG, Manning NJ, Kelly DE, Kelly SL et al. (2007). Lanosterol biosynthesis in the prokaryote Methylococcus capsulatus: insight into the evolution of sterol biosynthesis. Mol Biol Evol 24: 1714-1721.
22. Lasken R, Raghunathan A, Kvist T, Ishøy T, Westermann P, Ahring BK et al. (2005). Multiple displacement amplification of genomic DNA. In: Hughes, S, Lasken, R (eds). Whole Genome Amplification: Methods Express. Scion Publishing: Banbury, pp 119-147.
23. Li CW, Chen JY, Hua TE. (1998). Precambrian sponges with cellular structures. Science 279: 879-882.
24. Love GD, Grosjean E, Stalvies C, Fike DA, Grotzinger JP, Bradley AS et al. (2009). Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457: 718-721.
25. Lowe TM, Eddy SR. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
26. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
27. Marcy Y, Ishoey T, Lasken RS, Stockwell TB, Walenz BP, Halpern AL et al. (2007). Nanoliter reactors improve multiple displacement amplification of genomes from single cells. PLoS Genet 3: 1702-1708.
28. Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J et al. (2003). GenDB - an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31: 2187-2195.
29. Minnikin DE, Kremer L, Dover LG, Besra GS. (2002). The methyl-branched fortifications of Mycobacterium tuberculosis. Chem Biol 9: 545-553.
30. Mussmann M, Hu FZ, Richter M, de Beer D, Preisler A, Jørgensen BB et al. (2007). Insights into the genome of large sulfur bacteria revealed by analysis of single filaments. PLoS Biol 5: e230.
31. Noguchi H, Park J, Takagi T. (2006). MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 33: 5623-5630.
32. Parada M, Vinardell JM, Ollero FJ, Hidalgo A, Gutiérrez R, Buendía-Clavería AMet al. (2006). Sinorhizobium fredii HH103 mutants affected in capsular polysaccharide (KPS) are impaired for nodulation with soybean and Cajanus cajan. Mol Plant Microbe Interact 19: 43-52.
33. Pearson A, Budin M, Brocks JJ. (2003). Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 100: 15352-15357.
34. Pham VD, Konstantinidis KT, Palden T, DeLong EF. (2008). Phylogenetic analyses of ribosomal DNAcontaining bacterioplankton genome fragments from a 4000 m vertical profile in the North Pacific Subtropical Gyre. Environ Microbiol 10: 2313-2330.
35. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
36. Quast C. (2006). MicHanThi - design and implementation of a system for the prediction of gene functions in genome annotation projects. Diploma thesis, University of Bremen.
37. Raghunathan A, Ferguson Jr HR, Bornarth CJ, Song W, Driscoll M, Lasken RS. (2005). Genomic DNA amplification from a single bacterium. Appl Environ Microbiol 71: 3342-3347.
38. 2 fixation. Biochim Biophys Acta 1784: 1873-1898.
39. Rappe MS, Giovannoni SJ. (2003). The uncultured microbial majority. Annu Rev Microbiol 57: 369-394.
40. RichterM, Lombardot T, Kostadinov I, Kottmann R, Duhaime MB, Peplies J et al. (2008). Jcoast - a biologist-centric software tool for data mining and comparison of prokaryotic (meta)genomes. BMC Bioinformatics 9: 177.
41. Rodrigue S, Malmstrom RR, Berlin AM, Birren BW, Henn MR, Chisholm SW. (2009). Whole genome amplification and de novo assembly of single bacterial cells. PLoS One 4: e6864.
42. Santarella-Mellwig R, Franke J, Jaedicke A, Gorjanacz M, Bauer U, Budd A et al. (2010). The compartmentalized bacteria of the Planctomycetes- Verrucomicrobia-Chlamydiae superphylum have membrane coat-like proteins. PloS Biol 8: e1000281.
43. 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 Microbiol 74: 7694-7708.
44. Siegl A, Hentschel U. (2009). PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ Microbiol Reports; e-pub ahead of print 31 July 2009, doi: 10.1111/j.1758-2229. 2009.00057.x.
45. Stepanauskas R, Sieracki ME. (2007). Matching phylogeny and metabolism in the uncultured marine bacteria, one cell at a time. Proc Natl Acad Sci USA 104: 9052-9057.
46. Taylor MW, Radax R, Steger D, Wagner M. (2007a). Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
47. Taylor MW, Thacker RT, Hentschel U. (2007b). Genetics. Evolutionary insights from sponges. Science 316: 1854-1855.
48. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A et al. (2010). Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J; e-pub ahead of print 3 June 2010, doi:10.1038/ismej.2010.74.
49. Wagner M, Horn M. (2006). The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17: 241-249.
50. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S et al. (2009). Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol; e-pub ahead of print 29 September 2009, doi: 10.1111/j.1462-2920.2009.02065.x.
51. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V et al. (2007). Database resources of the National Center for Biotechnology. Nucleic Acids Res 35: D5-D12.
52. Woyke T, Tighe D, Mavromatis K, Clum A, Copeland A, Schackwitz W et al. (2010). One bacterial cell, one complete genome. PLoS One 5: e10314.
53. Woyke T, Xie G, Copeland A, González JM, Han C, Kiss H et al. (2009). Assembling the marine metagenome, one cell at a time. PLoS One 4: e5299.
54. Zhang K, Martiny AC, Reppas NB, Barry KW, Malek J, Chisholm SW et al. (2006). Sequencing genomes from single cells by polymerase cloning. Nat Biotechnol 24: 680-686.