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Antonie van Leeuwenhoek

, Volume 112, Issue 8, pp 1231–1243 | Cite as

Assessment of Rhodopirellula rubra as a supplementary and nutritional food source to the microcrustacean Daphnia magna

  • Maria da Conceição Marinho
  • Olga Maria LageEmail author
  • Carla D. Sousa
  • José Catita
  • Sara C. AntunesEmail author
Original Paper
  • 73 Downloads

Abstract

The daily use of the planctomycete Rhodopirellula rubra as an alternative or supplementary food source for Daphnia magna and its feasibility in the nutrition of transgenerational populations were studied. The life history parameters, fatty acids (saturated, mono- and polyunsaturated; SFAs, MUFAs and PUFAs), glycogen and protein contents of organisms during feeding assays and of the first generation were analysed. An increase in the yields of D. magna with the increase of the cell concentration of R. rubra was evident, but overall, bacteria supplied as the only food source was nutritionally insufficient as observed for all the parameters analysed. However, when R. rubra was added as supplement to the microalgae Raphidocelis subcapitata a significant improvement in the life history parameters was observed namely in the reproductive output and the somatic growth rate. The identified SFAs, MUFAs and PUFAs were the fatty acids more abundant in daphniids, and the feed regimens influenced daphniids fatty acid profiles. Additionally, the mixed diet resulted in a larger number and size of offspring in the different F1 broods as also observed with the results of F0 generation. The pink colouration present in D. magna body and eggs confirmed that bacteria were absorbed, the pigment(s) retained and passed on to the next generation. Our results showed that R. rubra can play an essential role in D. magna diet as a nutritional supplement showing potential biotechnological applications.

Keywords

Daphnia Planctomycetes Rhodopirelulla rubra Fatty acids Glycogen Protein Fecundity 

Notes

Acknowledgements

Sara C. Antunes received a post doc grant (SFRH/BPD/109951/2015) by the Portuguese Foundation for Science and Technology (FCT). This research was partially supported by CIIMAR through the Strategic Funding UID/Multi/04423/2013 through national funds provided by FCT—Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020.

Authors’ contribution

MCM: experimental work and drafting of the manuscript; OML: design of the experimental work, experimental work and drafting and final revision of the manuscript; CDS: experimental work; JC: experimental work and drafting and final revision of the manuscript; SCA: design of the experimental work, experimental work and drafting and final revision of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or non-arthropod animals performed by any of the authors.

References

  1. Anderson BG, Jenkins JC (1942) A time study of events in the life span of Daphnia magna. Biol Bull 83:260–272.  https://doi.org/10.2307/1538146 CrossRefGoogle Scholar
  2. Antunes SC, Almeida RA, Carvalho T, Lage OM (2016) Feasibility of Planctomycetes as a nutritional or supplementary food source for Daphnia spp. Ann Limnol-Int J Lim 52:317–325.  https://doi.org/10.1051/limn/2016019 CrossRefGoogle Scholar
  3. ASTM (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E 729-80. American Society for Testing and Materials, PhiladelphiaGoogle Scholar
  4. ASTM (1997) Standard guide for conducting Daphnia magna life-cycle toxicity tests. Report E 1193-97. American Society for Testing and Materials, PhiladelphiaGoogle Scholar
  5. Baird DJ, Barber I, Bradley M, Calow P, Soares AMVM (1989a) The Daphnia bioassay: a critique. Hydrobiologia 188:403–406.  https://doi.org/10.1007/BF00027806 CrossRefGoogle Scholar
  6. Baird DJ, Soares AMVM, Girling A, Barber I, Bradley MC, Calow P (1989b) The long-term maintenance of Daphnia magna Straus for use in ecotoxicity tests: problems and prospects. In: Proceedings of the first European conference on ecotoxicology. Lyngby, pp 144–148Google Scholar
  7. Beatrici AC, Arenzon A, Coimbra NJ, Raya-Rodriguez MT (2006) Fertilidade e sensibilidade de Daphnia similis e Daphnia magna submetidas a diferentes cultivos. J Braz Soc Ecotoxicol 1:123–126CrossRefGoogle Scholar
  8. Becker C, Boersma M (2005) Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction. Limnol Oceanogr 50:388–397.  https://doi.org/10.4319/lo.2005.50.1.0388 CrossRefGoogle Scholar
  9. Biddanda B, Ogdahl M, Cotner J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46:730–739.  https://doi.org/10.4319/lo.2001.46.3.0730 CrossRefGoogle Scholar
  10. Boedeker C, Schuler M, Reintjes G, Jeske O, van Teeseling MC, Jogler M, Rast P, Borchert D, Devos DP, Kucklick M, Schaffer M, Kolter R, van Niftrik L, Engelmann S, Amann R, Rohde M, Engelhardt H, Jogler C (2017) Determining the bacterial cell biology of Planctomycetes. Nat Commun 8:14853.  https://doi.org/10.1038/ncomms14853 CrossRefGoogle Scholar
  11. Boersma M (1997) Offspring size in Daphnia: does it pay to be overweight? In: Brancelj A, De Meester L, Spaak P (eds) Cladocera: the biology of model organisms. developments in hydrobiology, vol 126, pp 79–88.  https://doi.org/10.1007/978-94-011-4964-8_9
  12. Boersma M, Vijverberg J (1995) Synergistic effects of different food species on life-history traits of Daphnia galeata. Hydrobiologia 307:109–115.  https://doi.org/10.1007/BF00032002 CrossRefGoogle Scholar
  13. Bondoso J, Albuquerque L, Lobo-da-Cunha A, Da Costa MS, Harder J, Lage OM (2014) Rhodopirellula lusitana sp. nov. and Rhodopirellula rubra sp. nov., isolated from the surface of macroalgae. Syst Appl Microbiol 37:157–164.  https://doi.org/10.1016/j.syapm.2013.11.004 CrossRefGoogle Scholar
  14. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  15. Brett MT (1993) Resource quality effects on Daphnia longispina offspring fitness. J Plankton Res 15:403–412.  https://doi.org/10.1093/plankt/15.4.403 CrossRefGoogle Scholar
  16. Brett MT, Muller-Navarra DC, Sang-Kyu P (2000) Empirical analysis of the effect of phosphorus limitation on algal food quality for freshwater zooplankton. Limnol Oceanogr 45:1564–1575.  https://doi.org/10.4319/lo.2000.45.7.1564 CrossRefGoogle Scholar
  17. Burns CW (1968) The relationship between body size of filter-feeding Cladocera and the maximum size of particle ingested. Limnol Oceanogr 13:675–678.  https://doi.org/10.4319/lo.1968.13.4.0675 CrossRefGoogle Scholar
  18. Burns CW (1995) Effects of crowding and different food levels on growth and reproductive investment of Daphnia. Oecologia 101:234–244.  https://doi.org/10.1007/BF00317289 CrossRefGoogle Scholar
  19. Chen M, Chen F, Li J, Zhao B (2009) Effect of temperature and food on development and growth of Daphnia similoides (Cladocera: Daphniidae) from Lake Donghu. J Freshw Ecol 24:545–551.  https://doi.org/10.1080/02705060.2009.9664331 CrossRefGoogle Scholar
  20. Coakley CM, Nestoros E, Little TJ (2018) Testing hypotheses for maternal effects in Daphnia magna. J Evol Biol 31:211–216.  https://doi.org/10.1111/jeb.13206 CrossRefGoogle Scholar
  21. Darchambeau F, Faerovig PJ, Hessen DO (2003) How Daphnia copes with excess carbon in its food. Oecologia 136:336–346.  https://doi.org/10.1007/s00442-003-1283-7 CrossRefGoogle Scholar
  22. DeMott WR (1986) The role of taste in food selection by freshwater zooplankton. Oecologia 69:334–340.  https://doi.org/10.1007/BF00377053 CrossRefGoogle Scholar
  23. DeMott WR, Gulati RD, Siewertsen K (1998) Effects of phosphorus-deficient diets on the carbon and phosphorus balance of Daphnia magna. Limnol Oceanogr 43:1147–1161.  https://doi.org/10.4319/lo.1998.43.6.1147 CrossRefGoogle Scholar
  24. Ebert D (1993) The trade-off between offspring size and number in Daphnia magna: the influence of genetic, environmental and maternal effects. Arch Hydrobiol 90:453–473Google Scholar
  25. Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia. National Library of Medicine (US), National Center for Biotechnology Information, BethesdaGoogle Scholar
  26. Enserink EL, Kerkhofs MJJ, Baltus CAM, Koeman JH (1995) Influence of food quantity and lead exposure on maturation in Daphnia magna; evidence for a trade-off mechanism. Funct Ecol 9:175–185.  https://doi.org/10.2307/2390562 CrossRefGoogle Scholar
  27. Environment Canada (1992) Biological test method: growth inhibition test using the freshwater alga Selenastrum capricornutum. Report EPS1/RM/25, Environment Canada, OttawaGoogle Scholar
  28. Fink P, Pflitsch C, Marin K (2012) Dietary essential amino acids affect the reproduction of the keystone herbivore Daphnia pulex. PLoS ONE 7(10):1371.  https://doi.org/10.1371/annotation/6d71b282-8e08-43ba-bef7-7ad45cd48784 Google Scholar
  29. Freese HM, Martin-Creuzburg D (2013) Food quality of mixed bacteria–algae diets for Daphnia magna. Hydrobiologia 715:63–76.  https://doi.org/10.1007/s10750-012-1375-7 CrossRefGoogle Scholar
  30. Gabsi F, Glazier DS, Hammers-Wirtz M, Ratte HT, Preuss TG (2014) How do interactive maternal traits and environmental factors determine offspring size in Daphnia magna? Ann Limnol-Int J Lim 50:9–18.  https://doi.org/10.1051/limn/2013067 CrossRefGoogle Scholar
  31. Glazier DS (1992) Effects of food, genotype, and maternal size and age on offspring investment in Daphnia magna. Ecology 73:910–926.  https://doi.org/10.2307/1940168 CrossRefGoogle Scholar
  32. Glazier DS, Calow P (1992) Energy allocation rules in Daphnia magna: clonal and age differences in the effects of food limitation. Oecologia 90:540–549CrossRefGoogle Scholar
  33. Gliwicz ZM, Siedlar E (1980) Food size limitation and algae interfering with food collection in Daphnia. Arch Hydrobiol 88(2):155–177Google Scholar
  34. Green J (1954) Size and reproduction in Daphnia magna (Crustacea: Cladocera). Proc Zool Soc Lond 124:535–545.  https://doi.org/10.1111/j.1469-7998.1954.tb07796.x CrossRefGoogle Scholar
  35. Gude H (1988) Direct and indirect influences of crustacean zooplankton on bacterioplankton of Lake Constance. Hydrobiologia 159:63–73.  https://doi.org/10.1007/BF00007368 CrossRefGoogle Scholar
  36. Guisande C, Gliwicz ZM (1992) Egg size and clutch size in two Daphnia species grown at different food levels. J Plankton Res 14:997–1007.  https://doi.org/10.1093/plankt/14.7.997 CrossRefGoogle Scholar
  37. Hessen DO, Andersen T (1990) Bacteria as a source of phosphorus for zooplankton. Hydrobiologia 206:217–223.  https://doi.org/10.1007/BF00014087 CrossRefGoogle Scholar
  38. ISO 12966–2 (2017) Animal and vegetable fats and oils—Gas chromatography of fatty acid methyl esters—Part 2: preparation of methyl esters of fatty acids, GenevaGoogle Scholar
  39. Jurgens K, Arndt H, Rothhaupt KO (1994) Zooplankton-mediated changes of bacterial community structure. Microb Ecol 27:27–42.  https://doi.org/10.1007/BF00170112 CrossRefGoogle Scholar
  40. Kankaala P (1988) The relative importance of algae and bacteria as food for Daphnia longispina (Cladocera) in a polyhumic lake. Freshw Biol 19:285–296.  https://doi.org/10.1111/j.1365-2427.1988.tb00351.x CrossRefGoogle Scholar
  41. Lage OM, Bondoso J (2011) Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 78:366–375.  https://doi.org/10.1111/j.1574-6941.2011.01168.x CrossRefGoogle Scholar
  42. Lage OM, Bondoso J (2014) Planctomycetes and macroalgae, a striking association. Front Microbiol 5.  https://doi.org/10.3389/fmicb.2014.00267
  43. Lage OM, Bondoso J, Lobo-da-Cunha A (2013) Insights into the ultrastructural morphology of novel Planctomycetes. Antonie van Leeuwenhoe 104:467–476.  https://doi.org/10.1007/s10482-013-9969-2 CrossRefGoogle Scholar
  44. Lampert W (1981) Inhibitory and toxic effects of blue-green algae on Daphnia. Int Rev Hydrobiol 66:285–298.  https://doi.org/10.1002/iroh.19810660302 CrossRefGoogle Scholar
  45. Lewis MA, Maki AW (1981) Effects of water hardness and diet on productivity of Daphnia magna Straus. in laboratory culture. Hydrobiologia 85:175–179.  https://doi.org/10.1007/BF0000662 CrossRefGoogle Scholar
  46. Marinho MC, Lage OM, Catita J, Antunes SC (2017) Adequacy of Planctomycetes as supplementary food source for Daphnia magna. Anto Leeuw 111:825–840.  https://doi.org/10.1007/s10482-017-0997-1 CrossRefGoogle Scholar
  47. Martin-Creuzburg D, Von Elert E (2004) Impact of 10 dietary sterols on growth and reproduction of Daphnia galeata. J Chem Ecol 30:483–500.  https://doi.org/10.1023/B:JOEC.0000018624.94689.95 CrossRefGoogle Scholar
  48. Martin-Creuzburg D, Sperfeld E, Wacker A (2009) Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids. Proc R Soc Lond B: Biol Sci 276:1805–1814.  https://doi.org/10.1098/rspb.2008.1540 CrossRefGoogle Scholar
  49. Martin-Creuzburg D, Beck B, Freese HM (2011) Food quality of heterotrophic bacteria for Daphnia magna: evidence for a limitation by sterols. FEMS Microbiol Ecol 76:592–601.  https://doi.org/10.1111/j.1574-6941.2011.01076.x CrossRefGoogle Scholar
  50. Martins J, Teles LO, Vasconcelos V (2007) Assays with Daphnia magna and Danio rerio as alert systems in aquatic toxicology. Environ Int 33:414–425.  https://doi.org/10.1016/j.envint.2006.12.006 CrossRefGoogle Scholar
  51. McKee D, Ebert D (1996) The interactive effects of temperature, food level and maternal phenotype on offspring size in Daphnia magna. Oecologia 107:189–196CrossRefGoogle Scholar
  52. Meyer JS, Ingersoll CG, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife versus bootstrap techniques. Ecology 67:1156–1166.  https://doi.org/10.2307/1938671 CrossRefGoogle Scholar
  53. OECD (2006) Algal growth inhibition test. Guidelines for testing of chemicals, test guideline no 201, OECD (Organisation for Economic Cooperation and Development), ParisGoogle Scholar
  54. OECD (2012) Daphnia magna reproduction test, test guideline no 211, OECD (Organisation for Economic Cooperation and Development). ParisGoogle Scholar
  55. Pace ML, Porter KG, Feig YS (1983) Species and age specific differences in bacterial resource utilization by two co-occurring cladocerans. Ecology 64:1145–1156.  https://doi.org/10.2307/1937825 CrossRefGoogle Scholar
  56. Pace ML, McManus GB, Findlay SE (1990) Planktonic community structure determines the fate of bacterial production in a temperate lake. Limnol Oceanogr 35:795–808.  https://doi.org/10.4319/lo.1990.35.4.0795 CrossRefGoogle Scholar
  57. Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394CrossRefGoogle Scholar
  58. Shaw JR, Pfrender ME, Eads BD, Klaper R, Callaghan A, Sibly RM, Colson I, Jansen B, Gilbert D, Colbourne JK (2008) Daphnia as an emerging model for toxicological genomics. Adv Exp Biol 2:165–328.  https://doi.org/10.1016/S1872-2423(08)00005-7 CrossRefGoogle Scholar
  59. Siciliano A, Gesuele R, Pagano G, Guida M (2015) How Daphnia (Cladocera) assays may be used as bioindicators of health effects? J Biodivers Endanger Species S1:005.  https://doi.org/10.4172/2332-2543.S1.005 Google Scholar
  60. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506.  https://doi.org/10.1086/282929 CrossRefGoogle Scholar
  61. Stein JR (1973) Handbook of phycological methods—culture methods and growth measurements. Cambridge University Press, CambridgeGoogle Scholar
  62. Stollewerk A (2010) The water flea Daphnia—a ‘new’ model system for ecology and evolution? J Biol 9:21CrossRefGoogle Scholar
  63. Taipale SJ, Brett MT, Pulkkinen K, Kainz MJ (2012) The influence of bacteria-dominated diets on Daphnia magna somatic growth, reproduction, and lipid composition. FEMS Microbiol Ecol 82:50–62.  https://doi.org/10.1111/j.1574-6941.2012.01406.x CrossRefGoogle Scholar
  64. Tessier AJ, Leibold MA, Tsao J (2000) A fundamental trade-off in resource exploitation by Daphnia and consequences to plankton communities. Ecology 81:826–841.  https://doi.org/10.1890/0012-9658(2000)081%5b0826:AFTOIR%5d2.0.CO;2 CrossRefGoogle Scholar
  65. Urabe J, Sterner RW (2001) Contrasting effects of different types of resource depletion on life-history traits in Daphnia. Funct Ecol 15:165–174.  https://doi.org/10.1046/j.1365-2435.2001.00511.x CrossRefGoogle Scholar
  66. Vadstein O (2000) Heterotrophic, planktonic bacteria and cycling of phosphorus. In: Schink B. (ed) Adv Microb Ecol 16:115–167.  https://doi.org/10.1007/978-1-4615-4187-5_4
  67. Vijverberg J (1989) Culture techniques for studies on the growth, development and reproduction of copepods and cladocerans under laboratory and in situ conditions: a review. Freshw Biol 21:317–373.  https://doi.org/10.1111/j.1365-2427.1989.tb01369.x CrossRefGoogle Scholar
  68. Volkman J (2003) Sterols in microorganisms. Appl Microbiol Biotechnol 60:495–506.  https://doi.org/10.1007/s00253-002-1172-8 CrossRefGoogle Scholar
  69. 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.  https://doi.org/10.1016/j.copbio.2006.05.005 CrossRefGoogle Scholar
  70. Wenzel A, Bergstrom AK, Jansson M, Vrede T (2012) Survival, growth and reproduction of Daphnia galeata feeding on single and mixed Pseudomonas and Rhodomonas diets. Freshw Biol 57:835–846.  https://doi.org/10.1111/j.1365-2427.2012.02751.x CrossRefGoogle Scholar
  71. Wiegand S, Jogler M, Jogler C (2018) On the maverick Planctomycetes. FEMS Microbiol Rev 42:739–760.  https://doi.org/10.1093/femsre/fuy029 CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Departamento de Biologia da Faculdade de Ciências da Universidade do Porto (FCUP)PortoPortugal
  2. 2.Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR)Terminal de Cruzeiros do Porto de LeixõesMatosinhosPortugal
  3. 3.Paralab, SAValbomPortugal
  4. 4.CEBIMED - Faculdade de Ciências da Saúde da Universidade Fernando Pessoa (FCS-UFP)PortoPortugal

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