Implementing sponge physiological and genomic information to enhance the diversity of its culturable associated bacteria

FEMS Microbiology Ecology

Volumn 87, Issue 2, 2014, Pages 486-502

  Lavy, Adi ^a   Keren, Ray ^a   Haber, Markus ^a   Schwartz, Inbar ^a   Ilan, Micha ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Bacterial cultivation; Porifera; Sponge specific cluster; Symbionts; Theonella swinhoei

Indexed keywords

ANTIINFECTIVE AGENT; RNA 16S;

ANIMAL; ARTICLE; BACTERIAL CULTIVATION; BACTERIAL GENE; BACTERIUM; CLASSIFICATION; CULTURE MEDIUM; CULTURE TECHNIQUE; DNA SEQUENCE; GENETICS; GENOMICS; ISOLATION AND PURIFICATION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; RNA GENE; SPONGE (PORIFERA); SPONGE-SPECIFIC CLUSTER; SYMBIONT; THEONELLA SWINHOEI;

BACTERIAL CULTIVATION; PORIFERA; SPONGE-SPECIFIC CLUSTER; SYMBIONTS; THEONELLA SWINHOEI;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIOLOGICAL TECHNIQUES; BASE SEQUENCE; CELL CULTURE TECHNIQUES; CULTURE MEDIA; GENES, BACTERIAL; GENES, RRNA; GENOMICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84895076631     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12240     Document Type: Article

References (89)

1. Abdelmohsen UR, Pimentel-Elardo SM, Hanora A, Radwan M, Abou-El-Ela SH, Ahmed S & Hentschel U (2010) Isolation, phylogenetic analysis and anti-infective activity screening of marine sponge-associated actinomycetes. Mar Drugs 8: 399.
2. Aeschlimann A & Stockar U (1990) The effect of yeast extract supplementation on the production of lactic acid from whey permeate by Lactobacillus helueticus. Appl Microbiol Biotechnol 32: 398-402.
3. Ang KKH, Holmes MJ, Higa T, Hamann MT & Kara UAK (2000) In vivo antimalarial activity of the beta-carboline alkaloid Manzamine A. Antimicrob Agents Chemother 44: 1645-1649.
4. Ben-Dov E, Kramarsky-Winter E & Kushmaro A (2009) An in situ method for cultivating microorganisms using a double encapsulation technique. FEMS Microbiol Ecol 68: 363-371.
5. Bergman O (2009) Marine based cultivation of sponges and isolation of their associated bacteria, as first steps towards the accumulation of bioactive marine products. MSc Thesis, Tel Aviv University, Tel Aviv, Israel.
6. Bergman O, Mayzel B, Anderson MA, Shpigel M, Hill RT & Ilan M (2011) Examination of marine-based cultivation of three demosponges for acquiring bioactive marine natural products. Mar Drugs 9: 2201-2219.
7. Bewley CA, Holland ND & Faulkner DJ (1996) Two classes of metabolites from Theonella swinhoei are localized in distinct populations of bacterial symbionts. Experientia 52: 716-722.
8. Bollmann A, Lewis K & Epstein SS (2007) Incubation of environmental samples in a diffusion chamber increases the diversity of recovered isolates. Appl Environ Microbiol 73: 6386-6390.
9. Bruck WM, Bruck TB, Self WT, Reed JK, Nitecki SS & McCarthy PJ (2010) Comparison of the anaerobic microbiota of deep-water Geodia spp. and sandy sediments in the Straits of Florida. ISME J 4: 686-699.
10. Burrus V, Pavlovic G, Decaris B & Guedon G (2002) Conjugative transposons: the tip of the iceberg. Mol Microbiol 46: 601-610.
11. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11: 265-270.
12. Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM & Tiedje JM (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35: D169-D172.
13. Cole JR, Wang Q, Cardenas E et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
14. Darriba D, Taboada GL, Doallo R & Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9: 772.
15. DeLong EF (2005) Microbial community genomics in the ocean. Nat Rev Microbiol 3: 459-469.
16. Diaz MC & Ward BB (1997) Sponge-mediated nitrification in tropical benthic communities. Mar Ecol Prog Ser 156: 97-107.
17. Ellington WR & Suzuki T (2007) Early evolution of the creatine kinase gene family and the capacity for creatine biosynthesis and membrane transport. Subcell Biochem 46: 17-26.
18. Erwin PM, López-Legentil S & Schuhmann PW (2010) The pharmaceutical value of marine biodiversity for anti-cancer drug discovery. Ecol Econ 70: 445-451.
19. Erwin PM, Olson JB & Thacker RW (2011) Phylogenetic diversity, host-specificity and community profiling of sponge-associated bacteria in the northern Gulf of Mexico. PLoS ONE 6: e26806.
20. Fajardo A & Martínez JL (2008) Antibiotics as signals that trigger specific bacterial responses. Curr Opin Microbiol 11: 161-167.
21. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS & Thomas T (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. P Natl Acad Sci USA 109: E1878-E1887.
22. Fattorusso E & Taglialatela-Scafati O (2009) Marine antimalarials. Mar Drugs 7: 130-152.
23. Gilbert JA, Lee CK, Herbold CW, Polson SW, Wommack KE, Williamson SJ, McDonald IR & Cary SC (2012) Groundtruthing next-gen sequencing for microbial ecology - biases and errors in community structure estimates from PCR amplicon pyrosequencing. PLoS ONE 7: e44224.
24. Giovannoni S & Stingl U (2007) The importance of culturing bacterioplankton in the 'omics' age. Nat Rev Microbiol 5: 820-826.
25. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W & Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
26. Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C & Hacker J (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol 35: 305-312.
27. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J & Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68: 4431-4440.
28. Hentschel U, Usher KM & Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55: 167-177.
29. Hill TCJ, Walsh KA, Harris JA & Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43: 1-11.
30. Hoffmann F, Larsen O, Thiel V, Rapp HT, Pape T, Michaelis W & Reitner J (2005) An anaerobic world in sponges. Geomicrobiol J 22: 1-10.
31. Hoffmann F, Røy H, Bayer K, Hentschel U, Pfannkuchen M, Brümmer F & Beer D (2008) Oxygen dynamics and transport in the Mediterranean sponge Aplysina aerophoba. Mar Biol 153: 1257-1264.
32. Ilan M, Gugel J & Van Soest RWM (2004) Taxonomy, reproduction and ecology of new and known Red Sea sponges. Sarsia 89: 388-410.
33. Imhoff JF & Trüper HG (1976) Marine sponges as habitats of anaerobic phototrophic bacteria. Microb Ecol 3: 1-9.
34. Kaeberlein T, Lewis K & Epstein SS (2002) Isolating 'uncultivable' microorganisms in pure culture in a simulated natural environment. Science 296: 1127-1129.
35. Kaplan HB & Greenberg EP (1985) Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol 163: 1210-1214.
36. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP & Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464.
37. Kemp PF & Aller JY (2004) Estimating prokaryotic diversity: when are 16S rDNA libraries large enough? Limnol Oceanogr Methods 2: 114-125.
38. Kim TK, Garson MJ & Fuerst JA (2005) Marine actinomycetes related to the 'Salinospora' group from the Great Barrier Reef sponge Pseudoceratina clavata. Environ Microbiol 7: 509-518.
39. Kim OS, Cho YJ, Lee K et al. (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62: 716-721.
40. Kimura M, Wakimoto T, Egami Y, Tan KC, Ise Y & Abe I (2012) Calyxamides A and B, cytotoxic cyclic peptides from the marine sponge Discodermia calyx. J Nat Prod 75: 290-294.
41. Kunin V, Engelbrektson A, Ochman H & Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12: 118-123.
42. Leal MC, Puga J, Serôdio J, Gomes NCM & Calado R (2012) Trends in the discovery of new marine natural products from invertebrates over the last two decades - where and what are we bioprospecting? PLoS ONE 7: e30580.
43. Li ZY & Liu Y (2006) Marine sponge Craniella austrialiensis-associated bacterial diversity revelation based on 16S rDNA library and biologically active actinomycetes screening, phylogenetic analysis. Lett Appl Microbiol 43: 410-416.
44. Liu MY, Kjelleberg S & Thomas T (2011) Functional genomic analysis of an uncultured delta- proteobacterium in the sponge Cymbastela concentrica. ISME J 5: 427-435.
45. Ludwig W, Strunk O, Westram R et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
46. Madigan MT, Martinko JM & Parker J (2000) Brock Biology of Microorganisms. Prentice Hall College, London.
47. Maldonado M, Ribes M & van Duyl FC (2012) Nutrient fluxes through sponges: biology, budgets, and ecological implications. Advances in Sponge Science: Physiology, Chemical and Microbial Diversity, Biotechnology, Vol. 62 (Becerro MA, Uriz MJ, Maldonado M & Turon X, eds), pp. 113-182. Elsevier Academic Press Inc., San Diego, CA.
48. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Dymock D & Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64: 795-799.
49. Okada Y, Matsunaga S, van Soest RWM & Fusetani N (2002) Nagahamide A, an antibacterial depsipeptide from the marine sponge Theonella swinhoei. Org Lett 4: 3039-3042.
50. Olson JB, Lord CC & McCarthy PJ (2000) Improved recoverability of microbial colonies from marine sponge samples. Microb Ecol 40: 139-147.
51. Partida-Martinez LP, Groth I, Schmitt I, Richter W, Roth M & Hertweck C (2007a) Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microsporus. Int J Syst Evol Microbiol 57: 2583-2590.
52. Partida-Martinez LP, Flores de Looß C, Ishida K, Ishida M, Roth M, Buder K & Hertweck C (2007b) Rhizonin, the first mycotoxin isolated from the Zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl Environ Microbiol 73: 793-797.
53. Pedrós-Alió C (2012) The rare bacterial biosphere. Ann Rev Mar Sci 4: 449-466.
54. Piel J (2009) Metabolites from symbiotic bacteria. Nat Prod Rep 26: 338-362.
55. Piel J, Hui DQ, Wen GP, Butzke D, Platzer M, Fusetani N & Matsunaga S (2004) Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. P Natl Acad Sci USA 101: 16222-16227.
56. Pile AJ & Young CM (2006) The natural diet of a hexactinellid sponge: benthic-pelagic coupling in a deep-sea microbial food web. Deep Sea Res Part 1 Oceanogr Res Pap 53: 1148-1156.
57. Pruesse E, Peplies J & Glockner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28: 1823-1829.
58. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
59. Radjasa OK, Vaske YM, Navarro G, Vervoort HC, Tenney K, Linington RG & Crews P (2011) Highlights of marine invertebrate-derived biosynthetic products: their biomedical potential and possible production by microbial associants. Bioorg Med Chem 19: 6658-6674.
60. Ribes M, Coma R, Atkinson MJ & Kinzie RA (2005) Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. Limnol Oceanogr 50: 1480-1489.
61. Sakai R, Higa T, Jefford CW & Bernardinelli G (1986) Manzamine A, a novel antitumor alkaloid from a sponge. J Am Chem Soc 108: 6404-6405.
62. Schippers KJ, Sipkema D, Osinga R, Smidt H, Pomponi SA, Martens DE & Wijffels RH (2012) Cultivation of sponges, sponge cells and symbionts. Adv Mar Biol 62: 273-337.
63. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform- independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
64. Schmidt EW, Obraztsova AY, Davidson SK, Faulkner DJ & Haygood MG (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel delta-proteobacterium, 'Candidatus Entotheonella palauensis'. Mar Biol 136: 969-977.
65. Schmitt S, Tsai P, Bell J et al. (2012) Assessing the complex sponge microbiota: core, variable and species- specific bacterial communities in marine sponges. ISME J 6: 564-576.
66. Schonberg CHL, Hoffmann F & Gatti S (2003) Using microsensors to measure sponge physiology. Boll Mus Ist Biol Univ Genova 68: 593-604.
67. Selvin J, Gandhimathi R, Kiran G, Priya S, Ravji T & Hema T (2009) Culturable heterotrophic bacteria from the marine sponge Dendrilla nigra: isolation and phylogenetic diversity of actinobacteria. Helgol Mar Res 63: 239-247.
68. Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC & Martiny JBH (2008) It's all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10: 2200-2210.
69. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T & Hentschel U (2010) Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5: 61-70.
70. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T & Hentschel U (2011) Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5: 61-70.
71. Simister RL, Deines P, Botte ES, Webster NS & Taylor MW (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14: 517-524.
72. Simmons TL, Coates RC, Clark BR, Engene N, Gonzalez D, Esquenazi E, Dorrestein PC & Gerwick WH (2008) Biosynthetic origin of natural products isolated from marine microorganism-invertebrate assemblages. P Natl Acad Sci USA 105: 4587-4594.
73. Sipkema D, Schippers K, Maalcke WJ, Yang Y, Salim S & Blanch HW (2011) Multiple approaches to enhance the cultivability of bacteria associated with the marine sponge Haliclona (?gellius) sp. Appl Environ Microbiol 77: 2130-2140.
74. Steindler L, Huchon D, Avni A & Ilan M (2005) 16S rRNA phylogeny of sponge-associated cyanobacteria. Appl Environ Microbiol 71: 4127-4131.
75. Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S & Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6: 121-130.
76. Taylor MW, Radax R, Steger D & Wagner M (2007a) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
77. Taylor MW, Hill RT, Piel J, Thacker RW & Hentschel U (2007b) Soaking it up: the complex lives of marine sponges and their microbial associates. ISME J 1: 187-190.
78. Taylor MW, Hill RT & Hentschel U (2011) Meeting Report: 1st international symposium on sponge microbiology. Mar Biotechnol 13: 1057-1061.
79. Tindall BJ, Rossello-Mora R, Busse HJ, Ludwig W & Kampfer P (2009) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60: 249-266.
80. Van Pilsum JF, Stephens GC & Taylor D (1972) Distribution of creatine, guanidinoacetate and enzymes for their biosynthesis in the animal kingdom. Implications for phylogeny. Biochem J 126: 325-345.
81. Wang Q, Garrity GM, Tiedje JM & Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
82. Webster NS, Taylor MW, Behnam F, Lucker S, Rattei T, Whalan S, Horn M & Wagner M (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082.
83. Weisz JB, Lindquist N & Martens CS (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 155: 367-376.
84. Wilkinson CR & Fay P (1979) Nitrogen-fixation in coral-reef sponges with symbiotic cyanobacteria. Nature 279: 527-529.
85. Wyss M & Kaddurah-Daouk R (2000) Creatine and creatinine metabolism. Physiol Rev 80: 1107-1213.
86. Yahel G, Sharp JH, Marie D, Hase C & Genin A (2003) In situ feeding and element removal in the symbiont-bearing sponge Theonella swinhoei: bulk DOC is the major source for carbon. Limnol Oceanogr 48: 141-149.
87. Yarza P, Ludwig W, Euzéby J, Amann R, Schleifer K-H, Glöckner FO & Rosselló-Móra R (2010) Update of the All-Species Living Tree Project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33: 291-299.
88. Yousaf M, El Sayed KA, Rao KV et al. (2002) 12, 34-Oxamanzamines, novel biocatalytic and natural products from manzamine producing Indo-Pacific sponges. Tetrahedron 58: 7397-7402.
89. Zoetendal EG, Plugge CM, Akkermans ADL & de Vos WM (2003) Victivallis vadensis gen. nov., sp. nov., a sugar-fermenting anaerobe from human faeces. Int J Syst Evol Microbiol 53: 211-215.