Abstract
There is worldwide growing interest in the occurrence and diversity of metabolites used as chemical mediators in cross-kingdom interactions within aquatic systems. Bacteria produce metabolites to protect and influence the growth and life cycle of their eukaryotic hosts. In turn, the host provides a nutrient-enriched environment for the bacteria. Here, we discuss the role of waterborne chemical mediators that are responsible for such interactions in aquatic multi-partner systems, including algae or invertebrates and their associated bacteria. In particular, this review highlights recent advances in the chemical ecology of aquatic systems that support the overall ecological significance of signaling molecules across the prokaryote–eukaryote boundary (cross-kingdom interactions) for growth, development and morphogenesis of the host. We emphasize the value of establishing well-characterized model systems that provide the basis for the development of ecological principles that represent the natural lifestyle and dynamics of aquatic microbial communities and enable a better understanding of the consequences of environmental change and the most effective means of managing community interactions.
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References
Adnani N, Rajski SR, Bugni TS (2017) Symbiosis-inspired approaches to antibiotic discovery. Nat Prod Rep 34:784–814. https://doi.org/10.1039/C7NP00009J
Alegado RA et al (2012) A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals. eLife 1:e00013. https://doi.org/10.7554/eLife.00013
Alsufyani T, Weiss A, Wichard T (2017) Time course exo-metabolomic profiling in the green marine macroalga Ulva (Chlorophyta) for identification of growth phase-dependent biomarkers. Mar Drugs 15:14. https://doi.org/10.3390/md15010014
Amin SA et al (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101. https://doi.org/10.1038/nature14488
Beemelmanns C, Woznica A, Alegado RA, Cantley AM, King N, Clardy J (2014) Synthesis of the rosette-inducing factor RIF-1 and analogs. J Am Chem Soc 136:10210–10213. https://doi.org/10.1021/ja5046692
Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277. https://doi.org/10.2307/1540052
Bhalerao RP, Bennett MJ (2003) The case for morphogens in plants. Nat Cell Biol 5:939–943. https://doi.org/10.1038/ncb1103-939
Brunet T, King N (2017) The origin of animal multicellularity and cell differentiation. Dev Cell 43:124–140. https://doi.org/10.1016/j.devcel.2017.09.016
Cantley AM, Woznica A, Beemelmanns C, King N, Clardy J (2016) Isolation and synthesis of a bacterially produced inhibitor of rosette development in Choanoflagellates. J Am Chem Soc 138:4326–4329. https://doi.org/10.1021/jacs.6b01190
Cartwright P, Collins A (2007) Fossils and phylogenies: integrating multiple lines of evidence to investigate the origin of early major metazoan lineages. Integr Comp Biol 47:744–751. https://doi.org/10.1093/icb/icm071
Catania F et al (2017) The hologenome concept: we need to incorporate function. Theory Biosci 136:89–98. https://doi.org/10.1007/s12064-016-0240-z
Collins S, Bell G (2004) Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566–569. https://doi.org/10.1038/nature02945
Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90. https://doi.org/10.1038/nature04056
Cunningham CW, Buss LW, Anderson C (1991) Molecular and geologic evidence of shared history between hermit-crabs and the symbiotic genus Hydractina. Evolution 45:1301–1316. https://doi.org/10.2307/2409881
Damiani CC (2003) Reproductive costs of the symbiotic hydroid Hydractinia symbiolongicarpus (Buss and Yund) to its host hermit crab Pagurus longicarpus (Say). J Exp Mar Biol Ecol 288:203–222. https://doi.org/10.1016/S0022-0981(03)00005-4
Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K, King N (2011) Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev Biol 357:73–82. https://doi.org/10.1016/j.ydbio.2011.06.003
Di D-W, Zhang C, Luo P, An C-W, Guo G-Q (2016) The biosynthesis of auxin: how many paths truly lead to IAA? Plant Growth Regul 78:275–285. https://doi.org/10.1007/s10725-015-0103-5
Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Funct Ecol 2:131–139. https://doi.org/10.2307/2389687
Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol Rev 37:462–476. https://doi.org/10.1111/1574-6976.12011
Fairclough SR et al (2013) Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14:R15. https://doi.org/10.1186/gb-2013-14-2-r15
Freckelton ML, Nedved BT, Hadfield MG (2017) Induction of invertebrate larval settlement; different bacteria, different mechanisms? Sci Rep 7:42557. https://doi.org/10.1038/srep42557
Fries L (1974) Growth stimulation of axenic red algae by simple phenolic compounds. J Exp Mar Biol Ecol 15:1–9
Galun E (2010) Phytohormones and pattering: the role of hormones in plant archicture. World Scientific Publishing Company, London
Ghaderiardakani F, Coates JC, Wichard T (2017) Bacteria-induced morphogenesis of Ulva intestinalis and Ulva mutabilis (Chlorophyta): a contribution to the lottery theory FEMS. Microbiol Ecol 93:fix094. https://doi.org/10.1093/femsec/fix094
Goecke F, Thiel V, Wiese J, Labes A, Imhoff JF (2013) Algae as an important environment for bacteria - phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52:14–24. https://doi.org/10.2216/12-24.1.sl
Grueneberg J, Engelen AH, Costa R, Wichard T (2016) Macroalgal morphogenesis induced by waterborne compounds and bacteria in coastal seawater. PLoS One 11:e0146307. https://doi.org/10.1371/journal.pone.0146307
Guerrero R, Margulis L, Berlanga M (2013) Symbiogenesis: the holobiont as a unit of evolution. Int Microbiol 16:133–144. https://doi.org/10.2436/20.1501.01.188
Guo H, Rischer M, Sperfeld M, Weigel C, Menzel KD, Clardy J, Beemelmanns C (2017) Natural products and morphogenic activity of γ-Proteobacteria associated with the marine hydroid polyp Hydractinia echinata. Bioorg Med Chem 25:6088–6097. https://doi.org/10.1016/j.bmc.2017.06.053
Hadfield MG (2011) Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annu Rev Mar Sci 3:453–470. https://doi.org/10.1146/annurev-marine-120709-142753
Harder T, Campbell AH, Egan S, Steinberg PD (2012) Chemical Mediation of Ternary Interactions Between Marine Holobionts and Their Environment as Exemplified by the Red Alga Delisea pulchra. J Chem Ecol 38:442–450. https://doi.org/10.1007/s10886-012-0119-5
Harder T, Tebben J, Möller M, Schupp P (2018) Chapter 10. Chemical ecology of marine invertebrate larval settlement. In: Puglisi MP, Becerro MA (eds) Chemical ecology: the ecological impacts of marine natural products. CRC Press, Boca Raton
Helliwell KE, Collins S, Kazamia E, Purton S, Wheeler GL, Smith AG (2015) Fundamental shift in vitamin B12 eco-physiology of a model alga demonstrated by experimental evolution. ISME J 9:1446–1455. https://doi.org/10.1038/ismej.2014.230
Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10:641–654. https://doi.org/10.1038/nrmicro2839
Hester ER, Barott KL, Nulton J, Vermeij MJA, Rohwer FL (2015) Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J 10:1157
Huang Y, Callahan S, Hadfield MG (2012) Recruitment in the sea: bacterial genes required for inducing larval settlement in a polychaete worm. Sci Rep 2:228. https://doi.org/10.1038/srep00228
Hung OS, Lee OO, Thiyagarajan V, He HP, Xu Y, Chung HC, Qiu JW, Qian PY, (2009) Characterization of cues from natural multi-species biofilms that induce larval attachment of the polychaete Hydroides elegans. Aquat Biol 4:253–262. https://doi.org/10.3354/ab00110
Joint I, Tait K, Callow ME, Callow JA, Milton D, Williams P, Camara M (2002) Cell-to-cell communication across the prokaryote eukaryote boundary. Science 298:1207. https://doi.org/10.1126/science.1077075
Joint I, Tait K, Wheeler G (2007) Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos Trans R Soc Lond Ser B Biol Sci 362:1223–1233. https://doi.org/10.1098/rstb.2007.2047
Kazamia E et al (2012) Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ Microbiol 14:1466–1476. https://doi.org/10.1111/j.1462-2920.2012.02733.x
Kazamia E, Helliwell KE, Purton S, Smith AG (2016) How mutualisms arise in phytoplankton communities: building eco-evolutionary principles for aquatic microbes. Ecol Lett 19:810–822. https://doi.org/10.1111/ele.12615
Kessler RW, Weiss A, Kuegler S, Hermes C, Wichard T (2018) Macroalagal-bacterial interactions: role of dimethylsulfoniopropionate in microbial gardening by Ulva (Chlorophyta) Mol Ecol 27:1808–1819. https://doi.org/10.1111/mec.14472
Kitamura M, Koyama T, Nakano Y, Uemura D (2005) Corallinafuran and corallinaether, novel toxic compounds from crustose coralline red algae. Chem Lett 34:1272–1273. https://doi.org/10.1246/cl.2005.1272
Kline DI, Kuntz NM, Breitbart M, Knowlton N, Rohwer F (2006) Role of elevated organic carbon levels and microbial activity in coral mortality. Mar Ecol Prog Ser 314:119–125. https://doi.org/10.3354/meps314119
Kuhlisch C, Pohnert G (2015) Metabolomics in chemical ecology. Nat Prod Rep 32:937–955. https://doi.org/10.1039/c5np00003c
Lancelot C (1983) Factors affecting phytoplankton extracellular release in the southern bight of the North Sea. Mar Ecol Prog Ser 12:115–121. https://doi.org/10.3354/meps012115
Leitz T, Wagner T (1993) The marine bacterium Alteromonas espejiana induces metamorphosis of the hydroid Hydractinia echinata. Mar Biol 115:173–178. https://doi.org/10.1007/BF00346332
Lewis K (2001) Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999–1007. https://doi.org/10.1128/aac.45.4.999-1007.2001
Madsen JS, Røder HL, Russel J, Sørensen H, Burmølle M, Sørensen SJ (2016) Coexistence facilitates interspecific biofilm formation in complex microbial communities. Environ Microbiol 18:2565–2574. https://doi.org/10.1111/1462-2920.13335
Maruyama A, Maeda M, Simidu U (1986) Occurrence of plant hormone (cytokinin)-producing bacteria in the sea. J Appl Bacteriol 61:569–574. https://doi.org/10.1111/j.1365-2672.1986.tb01731.x
Matsuo Y, Imagawa H, Nishizawa M, Shizuri Y (2005) Isolation of an algal morphogenesis inducer from a marine bacterium. Science 307:1598
McFall-Ngai M et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110:3229–3236. https://doi.org/10.1073/pnas.1218525110
Meyer N, Bigalke A, Kaulfuss A, Pohnert G (2017) Strategies and ecological roles of algicidal bacteria. FEMS Microbiol Rev 41:880–889
Molloy EM, Hertweck C (2017) Antimicrobial discovery inspired by ecological interactions. Curr Opin Microbiol 39:121–127. https://doi.org/10.1016/j.mib.2017.09.006
Moran NA, Sloan DB (2015) The hologenome concept: helpful or hollow? PLoS Biol 13:e1002311. https://doi.org/10.1371/journal.pbio.1002311
Moran MA et al (2007) Ecological genomics of marine roseobacters. Appl Environ Microbiol 73:4559–4569. https://doi.org/10.1128/aem.02580-06
Mouchka ME, Hewson I, Harvell CD (2010) Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50:662–674. https://doi.org/10.1093/icb/icq061
Müller WA, Leitz T (2002) Metamorphosis in the Cnidaria. Can J Zool 80:1755–1771. https://doi.org/10.1139/z02-130
Myklestad SM (1995) Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Sci Total Environ 165:155–164. https://doi.org/10.1016/0048-9697(95)04549-g
Negri AP, Webster NS, Hill RT, Heyward AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser 223:121–131. https://doi.org/10.3354/meps223121
Olson ND, Ainsworth TD, Gates RD, Takabayashi M (2009) Diazotrophic bacteria associated with Hawaiian Montipora corals: diversity and abundance in correlation with symbiotic dinoflagellates. J Exp Mar Biol Ecol 371:140–146. https://doi.org/10.1016/j.jembe.2009.01.012
Ortlepp S, Pedpradap S, Dobretsov S, Proksch P (2008) Antifouling activity of sponge-derived polybrominated diphenyl ethers and synthetic analogues. Biofouling 24:201–208. https://doi.org/10.1080/08927010802008096
Paul C, Mausz MA, Pohnert G (2013) A co-culturing/metabolomics approach to investigate chemically mediated interactions of planktonic organisms reveals influence of bacteria on diatom metabolism. Metabolomics 9:349–359. https://doi.org/10.1007/s11306-012-0453-1
Plickert G, Frank U, Muller WA (2012) Hydractinia, a pioneering model for stem cell biology and reprogramming somatic cells to pluripotency. Int J Dev Biol 56:519–534. https://doi.org/10.1387/ijdb.123502gp
Provasoli L (1958) Effect of plant hormones on Ulva. Biol Bull 114:375–384
Puglisi MP, Sneed JM, Sharp KH, Ritson-Williams R, Paul VJ (2014) Marine chemical ecology in benthic environments. Nat Prod Rep 31:1510–1553. https://doi.org/10.1039/C4NP00017J
Ranf S, Scheel D, Lee J (2016) Challenges in the identification of microbe-associated molecular patterns in plant and animal innate immunity: a case study with bacterial lipopolysaccharide. Mol Plant Pathol 17:1165–1169. https://doi.org/10.1111/mpp.12452
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10. https://doi.org/10.3354/meps243001
Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. mbio 7:2 e01395–2 e01315. https://doi.org/10.1128/mBio.01395-15
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362. https://doi.org/10.1038/nrmicro1635
Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39. https://doi.org/10.1111/j.1462-2920.2009.02027.x
Sapp M, Schwaderer AS, Wiltshire KH, Hoppe HG, Gerdts G, Wichels A (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol 53:683–699. https://doi.org/10.1007/s00248-006-9162-5
Schütz A, Golbik R, Tittmann K, Svergun DI, Koch MHJ, Hubner G, Konig S (2003) Studies on structure-function relationships of indolepyruvate decarboxylase from Enterobacter cloacae, a key enzyme of the indole acetic acid pathway. Eur J Biochem 270:2322–2331. https://doi.org/10.1046/j.1432-1033.2003.03602.x
Segev E et al (2016) Dynamic metabolic exchange governs a marine algal-bacterial interaction. eLife 5:e17473. https://doi.org/10.7554/eLife.17473
Seyedsayamdost MR, Case RJ, Kolter R, Clardy J (2011) The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 3:331–335. https://doi.org/10.1038/nchem.1002
Seymour JR, Amin SA, Raina JB, Stocker R (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2:17065. https://doi.org/10.1038/nmicrobiol.2017.65
Shikuma NJ, Pilhofer M, Weiss GL, Hadfield MG, Jensen GJ, Newman DK (2014) Marine tubeworm metamorphosis induced by arrays of bacterial phage tail–like structures. Science 343:529–533
Shikuma NJ, Antoshechkin I, Medeiros JM, Pilhofer M, Newman DK (2016) Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling. Proc Natl Acad Sci USA 113:10097–10102. https://doi.org/10.1073/pnas.1603142113
Singh RP, Reddy CRK (2014) Seaweed-microbial interactions: key functions of seaweed-associated bacteria. FEMS Microbiol Ecol 88:213–230. https://doi.org/10.1111/1574-6941.12297
Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88. https://doi.org/10.1038/nature12860
Spoerner M, Wichard T, Bachhuber T, Stratmann J, Oertel W (2012) Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J Phycol 48:1433–1447. https://doi.org/10.1111/j.1529-8817.2012.01231.x
Steinert G, Whitfield S, Taylor MW, Thoms C, Schupp PJ (2014) Application of Diffusion Growth Chambers for the Cultivation of Marine Sponge-Associated Bacteria. Mar Biotechnol 16:594–603. https://doi.org/10.1007/s10126-014-9575-y
Straight PD, Kolter R (2009) Interspecies chemical communication in bacterial development. In: Annual review of microbiology, vol 63. Annual Review of Microbiology. pp 99-118. doi:https://doi.org/10.1146/annurev.micro.091208.073248
Tebben J et al (2011) Induction of larval metamorphosis of the coral Acropora millepora by tetrabromopyrrole isolated from a Pseudoalteromonas bacterium. PLoS One 6:e19082. https://doi.org/10.1371/journal.pone.0019082
Tebben J et al (2015) Chemical mediation of coral larval settlement by crustose coralline algae. Sci Rep 5:10803. https://doi.org/10.1038/srep10803
Technau U, Steele RE (2011) Evolutionary crossroads in developmental biology: Cnidaria. Development (Cambridge, England) 138:1447–1458. https://doi.org/10.1242/dev.048959
Theis KR et al. (2016) Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes mSystems 1:e00028–16. https://doi.org/10.1128/mSystems.00028-16
Turing A (1952) The chemical basis of differentiation. Philos Trans R Soc London Ser B 237:37–72
Uemura D, Kita M, Arimoto H, Kitamura M (2009) Recent aspects of chemical ecology: natural toxins, coral communities, and symbiotic relationships. Pure Appl Chem 81:1093–1111. https://doi.org/10.1351/pac-con-08-08-12
Wahl M, Goecke F, Labes A, Dobretsov S, Weinberger F (2012) The Second Skin: Ecological role of epibiotic biofilms on marine organisms. Front Microbiol 3:292. https://doi.org/10.3389/fmicb.2012.00292
Walter M (2016) Isolierung und Charakterisierung morphogenetischer Substanzen aus marinen Bakterien (Master Thesis). Friedrich Schiller University Jena, Germany, Master Thesis
Wang H, Tomasch J, Michael V, Bhuju S, Jarek M, Petersen J, Wagner-Döbler I (2015) Identification of genetic modules mediating the Jekyll and Hyde interaction of Dinoroseobacter shibae with the Dinoflagellate Prorocentrum minimum. Front Microbiol 6:1262
Wang R, Gallant É, Seyedsayamdost MR (2016) Investigation of the genetics and biochemistry of roseobacticide production in the Roseobacter clade bacterium Phaeobacter inhibens. mBio 7:e02118–e02115. https://doi.org/10.1128/mBio.02118-15
Webster NS, Thomas T (2016) The sponge hologenome. mbio 7:e00135–e00116. https://doi.org/10.1128/mBio.00135-16
Weismann A (1883) Die Entstehung der Sexualzellen bei den Hydromedusen: Zugleich ein Beitrag zur Kenntniss des Baues und der Lebenserscheinungen dieser Gruppe. Fischer, Jena
Wichard T (2015) Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci 6:86. https://doi.org/10.3389/fpls.2015.00085
Wichard T (2016) Identification of metallophores and organic ligands in the chemosphere of the marine macroalga Ulva (Chlorophyta) and at land-sea interfaces. Front Mar Sci 3:131. https://doi.org/10.3389/fmars.2016.00131
Wichard T, Charrier B, Mineur F, Bothwell JH, De Clerck O, Coates JC (2015) The green seaweed Ulva: a model system to study morphogenesis. Front Plant Sci 6:72. https://doi.org/10.3389/fpls.2015.00072
Woodin SA, Marinelli RL, Lincoln DE (1993) Allelochemical inhibition of recruitment in a sedimentary assemblage. J Chem Ecol 19:517–530. https://doi.org/10.1007/BF00994322
Woznica A, King N (2018) Lessons from simple marine models on the bacterial regulation of eukaryotic development. Curr Opin Microbiol 43:108–116. https://doi.org/10.1016/j.mib.2017.12.013
Woznica A, Cantley AM, Beemelmanns C, Freinkman E, Clardy J, King N (2016) Bacterial lipids activate, synergize, and inhibit a developmental switch in choanoflagellates. Proc Natl Acad Sci USA 113:7894–7899. https://doi.org/10.1073/pnas.1605015113
Wu S, Shan L, He P (2014) Microbial signature-triggered plant defense responses and early signaling mechanisms. Plant Sci 228:118–126. https://doi.org/10.1016/j.plantsci.2014.03.001
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735. https://doi.org/10.1111/j.1574-6976.2008.00123.x
Acknowledgements
The authors are grateful for financial support from the Deutsche Forschungsgemeinschaft (DFG) for Grant SFB 1127 ChemBioSys (T.W., C.B.) and Exsphingo (C.B.). T.W. was also funded by the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska−Curie grant agreement No.642575—The ALgal Microbiome: Friends and Foes (ALFF). The authors were inspired by the vibrant COST Action FA1406 ‘Phycomorph’ Workshop in Jena (Germany) in 2017. We apologize to those colleagues whose work could not be cited owing to space constraints.
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Wichard, T., Beemelmanns, C. Role of Chemical Mediators in Aquatic Interactions across the Prokaryote–Eukaryote Boundary. J Chem Ecol 44, 1008–1021 (2018). https://doi.org/10.1007/s10886-018-1004-7
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DOI: https://doi.org/10.1007/s10886-018-1004-7