Skip to main content

Functional Transcripts Indicate Phylogenetically Diverse Active Ammonia-Scavenging Microbiota in Sympatric Sponges

Marine Biotechnology volume 20, pages 131–143 (2018)Cite this article

Abstract

Symbiotic ammonia scavengers contribute to effective removal of ammonia in sponges. However, the phylogenetic diversity and in situ activity of ammonia-scavenging microbiota between different sponge species are poorly addressed. Here, transcribed ammonia monooxygenase genes (amoA), hydrazine synthase genes (hzsA), and glutamine synthetase genes (glnA) were analyzed to reveal the active ammonia-scavenging microbiota in the sympatric sponges Theonella swinhoei, Plakortis simplex, and Phakellia fusca, and seawater. Archaeal amoA and bacterial glnA transcripts rather than bacterial amoA, hzsA, and archaeal glnA transcripts were detected in the investigated sponges and seawater. The transcribed amoA genes were ascribed to two Thaumarchaeota ecotypes, while the transcribed glnA genes were interspersed among the lineages of Cyanobacteria, Tectomicrobia, Poribacteria, Alpha-, Beta-, Gamma-, and Epsilonproteobacteria. In addition, transcribed abundances of archaeal amoA and bacterial glnA genes in these sponges have been quantified, showing significant variation among the investigated sponges and seawater. The transcriptome-based qualitative and quantitative analyses clarified the different phylogenetic diversity and transcription expression of functional genes related to microbially mediated ammonia scavenging in different sympatric sponges, contributing to the understanding of in situ active ecological functions of sponge microbial symbionts in holobiont nitrogen cycling.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Aoi Y, Masaki Y, Tsuneda S, Hirata A (2004) Quantitative analysis of amoA mRNA expression as a new biomarker of ammonia oxidation activities in a complex microbial community. Lett Appl Microbiol 39:477–482

    Article  CAS  PubMed  Google Scholar 

  • Bayer K, Moitinho-Silva L, Brummer F, Cannistraci CV, Ravasi T, Hentschel U (2014) GeoChip-based insights into the microbial functional gene repertoire of marine sponges (high microbial abundance, low microbial abundance) and seawater. FEMS Microbiol Ecol 90:832–843

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bouskill NJ, Eveillard D, Chien D, Jayakumar A, Ward BB (2012) Environmental factors determining ammonia-oxidizing organism distribution and diversity in marine environments. Environ Microbiol 14:714–729

    Article  CAS  PubMed  Google Scholar 

  • Christman GD, Cottrell MT, Popp BN, Gier E, Kirchman DL (2011) Abundance, diversity, and activity of ammonia-oxidizing prokaryotes in the coastal Arctic ocean in summer and winter. Appl Environ Microbiol 77:2026–2034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP (2005) Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 71:5362–5370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croue J, West NJ, Escande ML, Intertaglia L, Lebaron P, Suzuki MT (2013) A single betaproteobacterium dominates the microbial community of the crambescidine-containing sponge Crambe crambe. Sci Rep 3:2583

    Article  PubMed  PubMed Central  Google Scholar 

  • Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Damashek J, Smith JM, Mosier AC, Francis CA (2014) Benthic ammonia oxidizers differ in community structure and biogeochemical potential across a riverine delta. Front Microbiol 5:743

    PubMed  Google Scholar 

  • De Corte D, Yokokawa T, Varela MM, Agogue H, Herndl GJ (2009) Spatial distribution of Bacteria and Archaea and amoA gene copy numbers throughout the water column of the Eastern Mediterranean Sea. ISME J 3:147–158

    Article  PubMed  Google Scholar 

  • Diaz MC, Akob D, Cary CS (2004) Denaturing gradient gel electrophoresis of nitrifying microbes associated with tropical sponges. Boll Mus Ist Biol Univ Genova 68:279–289

    Google Scholar 

  • Diaz MC, Ward BB (1997) Sponge-mediated nitrification in tropical benthic communities. Mar Ecol Prog Ser 156:97–107

    Article  CAS  Google Scholar 

  • Dowle EJ, Pochon X, C Banks J, Shearer K, Wood SA (2016) Targeted gene enrichment and high-throughput sequencing for environmental biomonitoring: a case study using freshwater macroinvertebrates. Mol Ecol Resour 16:1240–1254

    Article  CAS  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci U S A 109:E1878–E1887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng G, Sun W, Zhang F, Karthik L, Li Z (2016) Inhabitancy of active Nitrosopumilus-like ammonia-oxidizing archaea and Nitrospira nitrite-oxidizing bacteria in the sponge Theonella swinhoei. Sci Rep 6:24966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiore CL, Baker DM, Lesser MP (2013) Nitrogen biogeochemistry in the Caribbean sponge, Xestospongia muta: a source or sink of dissolved inorganic nitrogen? PLoS One 8:e72961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:364

    Article  PubMed  PubMed Central  Google Scholar 

  • Forchhammer K (2007) Glutamine signalling in bacteria. Front Biosci 12:13

    Article  Google Scholar 

  • Fredriksson NJ, Hermansson M, Wilen BM (2013) The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PLoS One 8:e76431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeman CJ, Thacker RW, Baker DM, Fogel ML (2013) Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance? ISME J 7:1116–1125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganesh S, Bristow LA, Larsen M, Sarode N, Thamdrup B, Stewart FJ (2015) Size-fraction partitioning of community gene transcription and nitrogen metabolism in a marine oxygen minimum zone. ISME J 9:2682–2696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235

    Article  CAS  PubMed  Google Scholar 

  • Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, Sugahara J, Preston C, De La Torre J, Richardson PM, Delong EF (2006) Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci U S A 103:18296–18301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han M, Liu F, Zhang F, Li Z, Lin H (2012) Bacterial and archaeal symbionts in the South China Sea sponge Phakellia fusca: community structure, relative abundance, and ammonia-oxidizing populations. Mar Biotechnol (NY) 14:701–713

    Article  CAS  Google Scholar 

  • Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, Schlappy ML, Schleper C, Kuypers MM (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11:2228–2243

    Article  CAS  PubMed  Google Scholar 

  • Horak RE, Qin W, Schauer AJ, Armbrust EV, Ingalls AE, Moffett JW, Stahl DA, Devol AH (2013) Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by Archaea. ISME J 7:2023–2033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurt RA, Qiu X, Wu L, Roh Y, Palumbo AV, Tiedje JM, Zhou J (2001) Simultaneous recovery of RNA and DNA from soils and sediments. Appl Environ Microbiol 67:4495–4503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izumi H, Sagulenko E, Webb RI, Fuerst JA (2013) Isolation and diversity of planctomycetes from the sponge Niphates sp., seawater, and sediment of Moreton Bay, Australia. Antonie Van Leeuwenhoek 104:533–546

    Article  CAS  PubMed  Google Scholar 

  • Jiménez E, Ribes M (2007) Sponges as a source of dissolved inorganic nitrogen: nitrification mediated by temperate sponges. Limnol Oceanogr 52:948–958

    Article  Google Scholar 

  • Jing H, Xia X, Liu H, Zhou Z, Wu C, Nagarajan S (2015) Anthropogenic impact on diazotrophic diversity in the mangrove rhizosphere revealed by nifH pyrosequencing. Front Microbiol 6:1172

    Article  PubMed  PubMed Central  Google Scholar 

  • Jouett NJ, Bibbings ME, Sullivan CE, Parsons RJ (2015) Molecular investigation of the microbial community associated with the fire sponge, Tedania ignis, in Bermuda. PeerJ PrePrints 3:e1117

    Google Scholar 

  • Kong L, Jing H, Kataoka T, Buchwald C, Liu H (2013) Diversity and spatial distribution of hydrazine oxidoreductase (hzo) gene in the oxygen minimum zone off Costa Rica. PLoS One 8:e78275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuypers MM, Sliekers AO, Lavik G, Schmid M, Jorgensen BB, Kuenen JG, Sinninghe Damste JS, Strous M, Jetten MS (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422:608–611

    Article  CAS  PubMed  Google Scholar 

  • Li M, Hong Y, Klotz MG, Gu JD (2010) A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl Microbiol Biotechnol 86:781–790

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Wang Y, Li J, Liu F, He L, He Y, Wang S (2016) Metagenomic analysis of genes encoding nutrient cycling pathways in the microbiota of deep-sea and shallow-water sponges. Mar Biotechnol (NY) 18:659–671

    Article  CAS  Google Scholar 

  • Li ZY, Wang YZ, He LM, Zheng HJ (2014) Metabolic profiles of prokaryotic and eukaryotic communities in deep-sea sponge Neamphius huxleyi indicated by metagenomics. Sci Rep 4:3895

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu M, Fan L, Zhong L, Kjelleberg S, Thomas T (2012) Metaproteogenomic analysis of a community of sponge symbionts. ISME J 6:1515–1525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynn TM, Ge T, Yuan H, Wei X, Wu X, Xiao K, Kumaresan D, Yu SS, Wu J, Whiteley AS (2017) Soil carbon-fixation rates and associated bacterial diversity and abundance in three natural ecosystems. Microb Ecol 73:645–657

  • Mcclintock JB, Amsler CD, Baker BJ, Van Soest RW (2005) Ecology of antarctic marine sponges: an overview. Integr Comp Biol 45:359–368

    Article  PubMed  Google Scholar 

  • Mohamed NM, Enticknap JJ, Lohr JE, Mcintosh SM, Hill RT (2008) Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Appl Environ Microbiol 74:1209–1222

    Article  CAS  PubMed  Google Scholar 

  • Mohamed NM, Saito K, Tal Y, Hill RT (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4:38–48

    Article  CAS  PubMed  Google Scholar 

  • Moitinho-Silva L, Seridi L, Ryu T, Voolstra CR, Ravasi T, Hentschel U (2014) Revealing microbial functional activities in the Red Sea sponge Stylissa carteri by metatranscriptomics. Environ Microbiol 16:3683–3698

    Article  CAS  PubMed  Google Scholar 

  • Morrison DA (2007) Increasing the efficiency of searches for the maximum likelihood tree in a phylogenetic analysis of up to 150 nucleotide sequences. Syst Biol 56:988–1010

    Article  CAS  PubMed  Google Scholar 

  • Ozturk B, De Jaeger L, Smidt H, Sipkema D (2013) Culture-dependent and independent approaches for identifying novel halogenases encoded by Crambe crambe (marine sponge) microbiota. Sci Rep 3:2780

    Article  PubMed  PubMed Central  Google Scholar 

  • Pal S, Gregory-Eaves I, Pick FR (2015) Temporal trends in cyanobacteria revealed through DNA and pigment analyses of temperate lake sediment cores. J Paleolimnol 54:87–101

    Article  Google Scholar 

  • Paulot F, Jacob DJ, Johnson MT, Bell TG, Baker AR, Keene WC, Lima ID, Doney SC, Stock CA (2015) Global oceanic emission of ammonia: constraints from seawater and atmospheric observations. Glob Biogeochem Cycles 29:1165–1178

    Article  CAS  Google Scholar 

  • Perini F, Casabianca A, Battocchi C, Accoroni S, Totti C, Penna A (2011) New approach using the real-time PCR method for estimation of the toxic marine dinoflagellate Ostreopsis cf. ovata in marine environment. PLoS One 6:e17699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pimentel-Elardo S, Wehrl M, Friedrich AB, Jensen PR, Hentschel U (2003) Isolation of planctomycetes from Aplysina sponges. Aquat Microb Ecol 33:239–245

    Article  Google Scholar 

  • Polonia AR, Cleary DF, Freitas R, De Voogd NJ, Gomes NC (2015) The putative functional ecology and distribution of archaeal communities in sponges, sediment and seawater in a coral reef environment. Mol Ecol 24:409–423

    Article  CAS  PubMed  Google Scholar 

  • Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radax R, Hoffmann F, Rapp HT, Leininger S, Schleper C (2012a) Ammonia-oxidizing archaea as main drivers of nitrification in cold-water sponges. Environ Microbiol 14:909–923

    Article  CAS  PubMed  Google Scholar 

  • Radax R, Rattei T, Lanzen A, Bayer C, Rapp HT, Urich T, Schleper C (2012b) Metatranscriptomics of the marine sponge Geodia barretti: tackling phylogeny and function of its microbial community. Environ Microbiol 14:1308–1324

    Article  CAS  PubMed  Google Scholar 

  • Regnault M (1987) Nitrogen excretion in marine and fresh-water crustacea. Biol Rev 62:1–24

    Article  Google Scholar 

  • 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 8:1198–1209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rose TM, Henikoff JG, Henikoff S (2003) CODEHOP (COnsensus-DEgenerate Hybrid Oligonucleotide Primer) PCR primer design. Nucleic Acids Res 31:3763–3766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rua CP, Gregoracci GB, Santos EO, Soares AC, Francini-Filho RB, Thompson F (2015) Potential metabolic strategies of widely distributed holobionts in the oceanic archipelago of St Peter and St Paul (Brazil). FEMS Microbiol Ecol 91:fiv043

    Article  PubMed  Google Scholar 

  • Schirmer A, Gadkari R, Reeves CD, Ibrahim F, Delong EF, Hutchinson CR (2005) Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl Environ Microbiol 71:4840–4849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlappy ML, Schottner SI, Lavik G, Kuypers MM, De Beer D, Hoffmann F (2010) Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol 157:593–602

    Article  PubMed  Google Scholar 

  • 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 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MM, Pommerening-Roeser A, Op Den Camp HJ, Jetten MS (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10:3140–3149

    Article  CAS  PubMed  Google Scholar 

  • 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 6:564–576

    Article  CAS  PubMed  Google Scholar 

  • Sintes E, Bergauer K, De Corte D, Yokokawa T, Herndl GJ (2013) Archaeal amoA gene diversity points to distinct biogeography of ammonia-oxidizing Crenarchaeota in the ocean. Environ Microbiol 15:1647–1658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sintes E, De Corte D, Haberleitner E, Herndl GJ (2016) Geographic distribution of archaeal ammonia oxidizing ecotypes in the Atlantic Ocean. Front Microbiol 7:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Southwell MW, Weisz JB, Martens CS, Lindquist N (2008) In situ fluxes of dissolved inorganic nitrogen from the sponge community on Conch Reef, Key Largo, Florida. Limnol Oceanogr 53:986

    Article  CAS  Google Scholar 

  • Stark JM, Firestone MK (1996) Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol Biochem 28:1307–1317

    Article  CAS  Google Scholar 

  • Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, De Nys R, Wagner M, Taylor MW (2008) Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol 10:1087–1094

    Article  CAS  PubMed  Google Scholar 

  • Tahon G, Tytgat B, Stragier P, Willems A (2016) Analysis of cbbL, nifH, and pufLM in soils from the Sor Rondane Mountains, Antarctica, reveals a large diversity of autotrophic and phototrophic bacteria. Microb Ecol 71:131–149

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thacker RW, Freeman CJ (2012) Sponge-microbe symbioses: recent advances and new directions. Adv Mar Biol 62:57–111

    Article  PubMed  Google Scholar 

  • Thiel V, Neulinger SC, Staufenberger T, Schmaljohann R, Imhoff JF (2007) Spatial distribution of sponge-associated bacteria in the Mediterranean sponge Tethya aurantium. FEMS Microbiol Ecol 59:47–63

    Article  CAS  PubMed  Google Scholar 

  • Thomas T, Moitinho-Silva L, Lurgi M, Bjork JR, Easson C, Astudillo-Garcia C, Olson JB, Erwin PM, Lopez-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L, Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW, Montoya JM, Hentschel U, Webster NS (2016) Diversity, structure and convergent evolution of the global sponge microbiome. Nat Commun 7:11870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:1557–1567

    Article  CAS  PubMed  Google Scholar 

  • Tian RM, Sun J, Cai L, Zhang WP, Zhou GW, Qiu JW, Qian PY (2016) The deep-sea glass sponge Lophophysema eversa harbors potential symbionts responsible for the nutrient conversions of carbon, nitrogen and sulfur. Environ Microbiol 18:2481–2494

    Article  CAS  PubMed  Google Scholar 

  • Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995

    Article  CAS  PubMed  Google Scholar 

  • Trindade-Silva AE, Rua C, Silva GG, Dutilh BE, Moreira AP, Edwards RA, Hajdu E, Lobo-Hajdu G, Vasconcelos AT, Berlinck RG, Thompson FL (2012) Taxonomic and functional microbial signatures of the endemic marine sponge Arenosclera brasiliensis. PLoS One 7:e39905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Kessel MA, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJ, Kartal B, Jetten MS, Lücker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559

    Article  PubMed  PubMed Central  Google Scholar 

  • Von Wintzingerode F, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Article  Google Scholar 

  • Wang J, Dong H, Wang W, Gu JD (2014) Reverse-transcriptional gene expression of anammox and ammonia-oxidizing archaea and bacteria in soybean and rice paddy soils of Northeast China. Appl Microbiol Biotechnol 98:2675–2686

    Article  CAS  PubMed  Google Scholar 

  • Webster NS, Thomas T (2016) The sponge hologenome. MBio 7:e00135–e00116

    Article  PubMed  PubMed Central  Google Scholar 

  • Weigel BL, Erwin PM (2015) Intraspecific variation in microbial symbiont communities of the sun sponge, Hymeniacidon heliophila, from intertidal and subtidal habitats. Appl Environ Microbiol 82:650–658

    Article  PubMed  Google Scholar 

  • Wiley GB, Kelly JA, Gaffney PM (2014) Use of next-generation DNA sequencing to analyze genetic variants in rheumatic disease. Arthritis Res Ther 16:490

    Article  PubMed  PubMed Central  Google Scholar 

  • Yahel G, Whitney F, Reiswig HM, Eerkes-Medrano DI, Leys SP (2007) In situ feeding and metabolism of glass sponges (Hexactinellida, Porifera) studied in a deep temperate fjord with a remotely operated submersible. Limnol Oceanogr 52:428–440

    Article  CAS  Google Scholar 

  • Yang Z, Li Z (2012) Spatial distribution of prokaryotic symbionts and ammoxidation, denitrifier bacteria in marine sponge Astrosclera willeyana. Sci Rep 2:528

    Article  PubMed  PubMed Central  Google Scholar 

  • Zehr JP, Kudela RM (2011) Nitrogen cycle of the open ocean: from genes to ecosystems. Annu Rev Mar Sci 3:197–225

    Article  Google Scholar 

  • Zhang F, Pita L, Erwin PM, Abaid S, Lopez-Legentil S, Hill RT (2014a) Symbiotic archaea in marine sponges show stability and host specificity in community structure and ammonia oxidation functionality. FEMS Microbiol Ecol 90:699–707

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Vicente J, Hill RT (2014b) Temporal changes in the diazotrophic bacterial communities associated with Caribbean sponges Ircinia stroblina and Mycale laxissima. Front Microbiol 5:561

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (41776138 and U1301131), the 6th China-Croatia Science and Technology cooperation committee program (No. 6–13), and Minhang Leading Talent Project.

Author information

Authors and Affiliations

  1. State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Dongchuan Road 800, Shanghai, 200240, China

    Guofang Feng, Wei Sun, Fengli Zhang & Zhiyong Li

  2. Ruđer Bošković Institute, Bijeničkacesta 54, 10000, Zagreb, Croatia

    Sandi Orlić

  3. Center of Excellence for Science and Technology–Integration of Mediterranean region–STIM, Bijeničkacesta 54, 10000, Zagreb, Croatia

    Sandi Orlić

Authors
  1. Guofang Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fengli Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sandi Orlić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhiyong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhiyong Li.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic Supplementary Material

ESM 1

(DOCX 350 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Feng, G., Sun, W., Zhang, F. et al. Functional Transcripts Indicate Phylogenetically Diverse Active Ammonia-Scavenging Microbiota in Sympatric Sponges. Mar Biotechnol 20, 131–143 (2018). https://doi.org/10.1007/s10126-018-9797-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-018-9797-5

Keywords

  • Sponge
  • Ammonia-oxidizing archaea
  • Ammonia-assimilating bacteria
  • Functional transcript
  • RT-qPCR assays