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Marine Biotechnology

, Volume 18, Issue 6, pp 659–671 | Cite as

Metagenomic Analysis of Genes Encoding Nutrient Cycling Pathways in the Microbiota of Deep-Sea and Shallow-Water Sponges

  • Zhiyong LiEmail author
  • Yuezhu Wang
  • Jinlong Li
  • Fang Liu
  • Liming He
  • Ying He
  • Shenyue Wang
Original Article

Abstract

Sponges host complex symbiotic communities, but to date, the whole picture of the metabolic potential of sponge microbiota remains unclear, particularly the difference between the shallow-water and deep-sea sponge holobionts. In this study, two completely different sponges, shallow-water sponge Theonella swinhoei from the South China Sea and deep-sea sponge Neamphius huxleyi from the Indian Ocean, were selected to compare their whole symbiotic communities and metabolic potential, particularly in element transformation. Phylogenetically diverse bacteria, archaea, fungi, and algae were detected in both shallow-water sponge T. swinhoei and deep-sea sponge N. huxleyi, and different microbial community structures were indicated between these two sponges. Metagenome-based gene abundance analysis indicated that, though the two sponge microbiota have similar core functions, they showed different potential strategies in detailed metabolic processes, e.g., in the transformation and utilization of carbon, nitrogen, phosphorus, and sulfur by corresponding microbial symbionts. This study provides insight into the putative metabolic potentials of the microbiota associated with the shallow-water and deep-sea sponges at the whole community level, extending our knowledge of the sponge microbiota’s functions, the association of sponge- microbes, as well as the adaption of sponge microbiota to the marine environment.

Keywords

Sponge holobiont Metagenomics Metabolic profile Nutrient element 

Notes

Acknowledgments

Financial supports from the National Natural Science Foundation of China (NSFC) (U1301131, 41176127, 41076077) and Minhang Leading Talent Project are greatly acknowledged.

Compliance with Ethical Standards

Conflict of Interest

The authors declare no competing financial interests.

Supplementary material

10126_2016_9725_MOESM1_ESM.doc (1.8 mb)
ESM 1 (DOC 1.81 mb)

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  2. 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 10:2942–2955CrossRefPubMedGoogle Scholar
  3. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:141–145CrossRefGoogle Scholar
  4. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersenl GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefPubMedPubMedCentralGoogle Scholar
  5. Donia MS, Fricke WF, Partensky F, Cox J, Elshahawi SI, White JR, Phillippy AM, Schatz MC, Piel J, Haygood GM, Ravel J, Schmidt EW (2011) Complex microbiome underlying secondary and primary metabolism in the tunicate–Prochloron symbiosis. Proc Natl Acad Sci U S A 108:E1423–E1432CrossRefPubMedPubMedCentralGoogle Scholar
  6. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster N, Thomas T (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci U S A 109:E1878–E1887CrossRefPubMedPubMedCentralGoogle Scholar
  7. Fan L, Liu M, Simister R, Webster NS, Thomas T (2013) Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J 7:991–1002CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fiore CL, Labrie M, Jarett JK, Lesser MP (2015) Transcriptional activity of the giant barrel sponge, Xestospongia muta holobiont: molecular evidence for metabolic interchange. Front Microbiol 6:364CrossRefPubMedPubMedCentralGoogle Scholar
  9. Gao Z, Li B, Zheng C, Wang G (2008) Molecular detection of fungal communities in the Hawaiian marine sponges Suberites zeteki and Mycale armata. Appl Environ Microbiol 74:6091–6101CrossRefPubMedPubMedCentralGoogle Scholar
  10. Garson MJ, Flowers AE, Webb RI, Charan RD, McCaffrey EJ (1998) A sponge/dinoflagellate association in the haplosclerida sponge Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation. Cell Tissue Res 293:365–373CrossRefPubMedGoogle Scholar
  11. He L, Liu F, Karuppiah V, Ren Y, Li Z (2014) Comparisons of the fungal and protistan communities among different marine sponge holobionts by pyrosequencing. Microb Ecol 67:951–961CrossRefPubMedGoogle Scholar
  12. Huson DH, Mitra S, Weber N, Ruscheweyh H, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21:1552–1560CrossRefPubMedPubMedCentralGoogle Scholar
  13. Jin L, Liu F, Sun W, Zhang F, Karuppiah V, Li Z (2014) Pezizomycotina dominates the fungal communities of South China Sea sponges Theonella swinhoei and Xestospongia testudinaria. FEMS Microbiol Ecol 90:935–945CrossRefPubMedGoogle Scholar
  14. Kamke J, Sczyrba A, Ivanova N, Schwientek P, Rinke C, Mavromatis K, Woyke T, Hentschel U (2013a) Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges. ISME J 7:2287–2300CrossRefPubMedPubMedCentralGoogle Scholar
  15. Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30CrossRefPubMedPubMedCentralGoogle Scholar
  16. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25CrossRefPubMedPubMedCentralGoogle Scholar
  17. Lee OO, Wang Y, Yang J, Lafi FF, Al-Suwailem A, Qian P-Y (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 5:650–664CrossRefPubMedGoogle Scholar
  18. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079CrossRefPubMedPubMedCentralGoogle Scholar
  19. Li Z-Y, Wang Y-Z, He L-M, Zheng H-J (2014) Metabolic profiles of prokaryotic and eukaryotic communities in deep-sea sponge Neamphius huxleyi indicated by metagenomics. Sci Report 4:3895Google Scholar
  20. Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T (2012) Metaproteogenomic analysis of a community of sponge symbionts. ISME J 6:1515–1525CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lodwig EM, Hosie AHF, Bourdès A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS (2003) Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature 422:722–726CrossRefPubMedGoogle Scholar
  22. Lomsadze A, Ter-Hovhannisyan V, Chernoff Y, Borodovsky M (2005) Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res 33:6494–6506CrossRefPubMedPubMedCentralGoogle Scholar
  23. Maldonado M, Ribes M, van Duyl FC (2012) Nutrient fluxes through sponges: biology, budgets, and ecological implications. Adv Mar Biol 62:113–182CrossRefPubMedGoogle Scholar
  24. Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Marchler GH, Mullokandov M, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Yamashita RA, Yin JJ, Zhang D, Bryant SH (2005) CDD: a conserved domain database for protein classification. Nucleic Acids Res 33:192CrossRefGoogle Scholar
  25. Moitinho-Silva L, Seridi L, Ryu T, Voolstra CR, Ravasi T, Hentschel U (2014a) Revealing microbial functional activities in the Red Sea sponge Stylissa carteri by metatranscriptomics. Environ Microbiol 16:3683–3698CrossRefPubMedGoogle Scholar
  26. Moitinho-Silva L, Bayer K, Cannistraci CV, Giles EC, Ryu T, Seridi L, Ravasi T, Hentschel U (2014b) Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea. Mol Ecol 23:1348–1363CrossRefPubMedGoogle Scholar
  27. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628CrossRefPubMedGoogle Scholar
  28. Nichols SA (2005) An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Mol Phylogenet Evol 34:81–96CrossRefPubMedGoogle Scholar
  29. Noguchi H, Park J, Takagi T (2006) MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34:5623–5630CrossRefPubMedPubMedCentralGoogle Scholar
  30. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crécy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch GD, Rodionov DA, Rückert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y, Zagnitko O, Vonstein V (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:5691–5702CrossRefPubMedPubMedCentralGoogle Scholar
  31. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196CrossRefPubMedPubMedCentralGoogle Scholar
  32. Radax R, Rattei T, Lanzen A, Bayer C, Rapp HT, Urich T, Schleper C (2012) Metatranscriptomics of the marine sponge Geodia barretti: tackling phylogeny and function of its microbial community. Environ Microbiol 14:1308–1324CrossRefPubMedGoogle Scholar
  33. Reisser W (1984) The taxonomy of green algae endosymbiotic in ciliates and a sponge. Br Phycol J 19:309–318CrossRefGoogle Scholar
  34. Reveillaud J, Maignien L, Eren AM, Huber JA, Apprill A, Sogin ML, Vanreusel A (2014) Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J 8:1198–1209CrossRefPubMedPubMedCentralGoogle Scholar
  35. Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2:e92CrossRefPubMedPubMedCentralGoogle Scholar
  36. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  37. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, Webster N, Hentschel U, Taylor MW (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–574CrossRefPubMedGoogle Scholar
  38. Schnitzler CE, Weis VM (2010) Coral larvae exhibit few measurable transcriptional changes during the onset of coral–dinoflagellate endosymbiosis. Mar Genomics 3:107–116CrossRefPubMedGoogle Scholar
  39. Simister RL, Deines P, Botté ES, Webster NS, Taylor MW (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14:517–524CrossRefPubMedGoogle Scholar
  40. Smedile F, Messina E, La Cono V, Tsoy O, Monticelli LS, Borghini M, Giuliano L, Golyshin PN, Mushegian A, Yakimov MM (2013) Metagenomic analysis of hadopelagic microbial assemblages thriving at the deepest part of Mediterranean Sea, Matapan-Vavilov Deep. Environ Microbiol 15:167–182CrossRefPubMedGoogle Scholar
  41. Southwell MW, Weisz JB, Martens CS, Lindquist N (2008a) In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnol Oceanogr 53:986–996CrossRefGoogle Scholar
  42. Southwell MW, Popp BN, Martens CS (2008b) Nitrification controls on fluxes and isotopic composition of nitrate from Florida Keys sponges. Mar Chem 108:96–108CrossRefGoogle Scholar
  43. Steinert M, Hentschel U, Hacker J (2000) Symbiosis and pathogenesis: evolution of the microbe-host interaction. Naturwissenschaften 87:1–11CrossRefPubMedGoogle Scholar
  44. Taylor MW, Schupp PJ, Dahllöf I, Kjelleberg S, Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130CrossRefPubMedGoogle Scholar
  45. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347CrossRefPubMedPubMedCentralGoogle Scholar
  46. Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, Heidelberg KB, Egan S, Steinberg PD, Kjelleberg S (2010) Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J 4:1557–1567CrossRefPubMedGoogle Scholar
  47. Trindade-Silva AE, Rua C, Silva GGZ, Dutilh BE, Moreira APB, Edwards RA, Hajdu E, Lobo-Hajdu G, Vasconcelos AT, Berlinck RGS, Thompson FL (2012) Taxonomic and functional microbial signatures of the endemic marine sponge Arenosclera brasiliensis. PLoS One 7:e39905CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wang Q, Garrity GM, Tiedje JM, Cole J (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  49. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138CrossRefPubMedGoogle Scholar
  50. Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346CrossRefPubMedGoogle Scholar
  51. Webster NS, Taylor MW, Behnam F, Lücker 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 12:2070–2082PubMedPubMedCentralGoogle Scholar
  52. Woyke T, Xie G, Copeland A, González JM, Han C, Kiss H, Saw JH, Senin P, Yang C, Chatterji S, Cheng J-F, Eisen JA, Sieracki ME, Stepanauskas R (2009) Assembling the marine metagenome, one cell at a time. PLoS One 4:e5299CrossRefPubMedPubMedCentralGoogle Scholar
  53. Yu Z, Zhang B, Sun W, Zhang F, Li Z (2013) Phylogenetically diverse endozoic fungi in the South China Sea sponges and their potential in synthesizing bioactive natural products suggested by PKS gene and cytotoxic activity analysis. Fungal Divers 58:127–141CrossRefGoogle Scholar
  54. Zhang F, Blasiak LC, Karolin JO, Powell RJ, Geddes CD, Hill RT (2015a) Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges. Proc Natl Acad Sci U S A 112:4381–4386CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zhang D, Sun W, Feng G, Zhang F, Anbuchezhian R, Li Z, Jiang Q (2015b) Phylogenetic diversity of sulfate-reducing Desulfovibrio associated with three South China Sea sponges. Lett Appl Microbiol 60:504–512CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Zhiyong Li
    • 1
    Email author
  • Yuezhu Wang
    • 2
  • Jinlong Li
    • 1
  • Fang Liu
    • 1
  • Liming He
    • 1
  • Ying He
    • 3
  • Shenyue Wang
    • 2
  1. 1.Marine Biotechnology Laboratory, State Key Laboratory of Microbial Metabolism and School of Life Sciences and BiotechnologyShanghai Jiao Tong UniversityShanghaiPeople’s Republic of China
  2. 2.Shanghai-MOST Key Laboratory of Health and Disease GenomicsChinese National Human Genome Center at ShanghaiShanghaiPeople’s Republic of China
  3. 3.Laboratory of Marine Oceanography, State Key Laboratory of Microbial Metabolism and School of Life Sciences and BiotechnologyShanghai Jiao Tong UniversityShanghaiPeople’s Republic of China

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