Archives of Microbiology

, Volume 194, Issue 10, pp 879–885 | Cite as

Isolation and characterization of Planctomycetes from the sediments of a fish farm wastewater treatment tank

Original Paper

Abstract

The increasing ecological significance of Planctomycetes and the still limited knowledge of this group prompted us to obtain cultured isolates from the sediment of a treatment water recycling tank of a marine fish farm. Presence of strains from this group was assessed in the sediments and water column of the tank. Eleven isolates were obtained from the sediment sample by exploiting Planctomycetes natural resistance to several antibiotics and their capacity to degrade organic matter. Based on morphological characteristics and resistance to antibiotics, Planctomycetes were identified. Their phylogenetic affiliation was confirmed by the sequence analysis of the 16S rRNA gene that revealed the presence of a group of 6 isolates closely related to Rhodopirellula baltica and a cluster of 5 isolates with 97.7–97.9 % of similarity to this species, which probably are a different species of Rhodopirellula. ERIC-PCR profiles showed a higher discrimination within the two groups and allowed the identification of nine different genotypes within the isolated strains. This work corroborates the association of Rhodopirellula spp. with fish farm environments.

Keywords

Planctomycetes Rhodopirellula Isolation 16S rRNA Fish farm Wastewater 

References

  1. Bengtsson MM, Ovreas L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:261PubMedCrossRefGoogle Scholar
  2. Bengtsson MM, Sjøtun K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71–83CrossRefGoogle Scholar
  3. Bissett A, Bowman J, Burke C (2006) Bacterial diversity in organically-enriched fish farm sediments. FEMS Microbiol Ecol 55:48–56PubMedCrossRefGoogle Scholar
  4. Chelossi E, Vezzulli L, Milano A, Branzoni M, Fabiano M, Riccardi G, Banat IM (2003) Antibiotic resistance of benthic bacteria in fish-farm and control sediments of the Western Mediterranean. Aquaculture 219:83–97CrossRefGoogle Scholar
  5. Chipman L, Podgorski D, Green S, Kostka J, Cooper W, Huettel M (2010) Decomposition of plankton-derived dissolved organic matter in permeable coastal sediments. Limnol Oceanogr 55:857–871CrossRefGoogle Scholar
  6. Christensen PB, Rysgaard S, Sloth NP, Dalsgaard T, Schwaerter S (2000) Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aquat Microb Ecol 21:73–84CrossRefGoogle Scholar
  7. Cohen-Bazire G, Sistrom WR, Stanier RY (1957) Kinetic studies of pigment synthesis by non-sulphur purple bacteria. J Cell Comp Physiol 49:25–68CrossRefGoogle Scholar
  8. Cytryn E, van Rijn J, Schramm A, Gieseke A, de Beer D, Minz D (2005) Identification of bacteria potentially responsible for oxic and anoxic sulfide oxidation in biofilters of a recirculating mariculture system. Appl Environ Microbiol 71:6134–6141PubMedCrossRefGoogle Scholar
  9. DeLong EF, Franks DG, Alldredge L (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934CrossRefGoogle Scholar
  10. Deming JW, Baross JA (1993) The early diagenesis of organic matter: bacterial activity. In: Engel MH, Macko SA (eds) Organic geochemistry: principles and applications. Plenum Press, New York, pp 119–144CrossRefGoogle Scholar
  11. Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol 9:403–413. doi:10.1038/nrmicro2578 PubMedCrossRefGoogle Scholar
  12. Gade D, Gobom J, Rabus R (2005a) Proteomic analysis of carbohydrate catabolism and regulation in the marine bacterium Rhodopirellula baltica. Proteomics 5:3672–3683PubMedCrossRefGoogle Scholar
  13. Gade D, Stührmann T, Reinhardt R, Rabus R (2005b) Growth phase dependent regulation of protein composition in Rhodopirellula baltica. Environ Microbiol 7:1074–1084PubMedCrossRefGoogle Scholar
  14. Gao X-Y, Xu Y, Liu Y, Liu Z-P (2012) Bacterial diversity, community structure and function associated with biofilm development in a biological aerated filter in a recirculating marine aquaculture system. Mar Biodivers 1–11Google Scholar
  15. Glockner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, Gade D, Beck A, Borzym K, Heitmann K, Rabus R, Schlesner H, Amann R, Reinhardt R (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100:8298–8303PubMedCrossRefGoogle Scholar
  16. Hu YF, Fu CZ, Yin YS, Cheng G, Lei F, Yang X, Li J, Ashforth EJ, Zhang LX, Zhu BL (2010) Construction and preliminary analysis of a deep-sea sediment metagenomic fosmid library from Qiongdongnan Basin, South China Sea. Mar Biotechnol 12:719–727PubMedCrossRefGoogle Scholar
  17. Kawahara N, Shigematsu K, Miyadai T, Kondo R (2009) Comparison of bacterial communities in fish farm sediments along an organic enrichment gradient. Aquaculture 287:107–113CrossRefGoogle Scholar
  18. Kohler T, Stingl U, Meuser K, Brune A (2008) Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.). Environ Microbiol 10:1260–1270PubMedCrossRefGoogle Scholar
  19. Kummerer K (2009) Antibiotics in the aquatic environment—a review—part I. Chemosphere 75:417–434PubMedCrossRefGoogle Scholar
  20. Lachnit T, Meske D, Wahl M, Harder T, Schmitz R (2011) Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665PubMedCrossRefGoogle Scholar
  21. Lage OM, Bondoso J (2011) Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 78:366–375PubMedCrossRefGoogle Scholar
  22. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  23. Lonhienne TGA, Sagulenko E, Webb RI, Lee KC, Franke J, Devos DP, Nouwens A, Carroll BJ, Fuerst JA (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 107:12883–12888PubMedCrossRefGoogle Scholar
  24. Michaud L, Lo Giudice A, Troussellier M, Smedile F, Bruni V, Blancheton JP (2009) Phylogenetic characterization of the heterotrophic bacterial communities inhabiting a marine recirculating aquaculture system. J Appl Microbiol 107:1935–1946Google Scholar
  25. Mohan SB, Schmid M, Jetten M, Cole J (2004) Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiol Ecol 49:433–443PubMedCrossRefGoogle Scholar
  26. Musat N, Werner U, Knittel K, Kolb S, Dodenhof T, van Beusekom JEE, de Beer D, Dubilier N, Amann R (2006) Microbial community structure of sandy intertidal sediments in the North Sea, Sylt-Rømø Basin, Wadden Sea. Syst Appl Microbiol 29:333–348PubMedCrossRefGoogle Scholar
  27. Nelson KE et al (2010) A catalog of reference genomes from the human microbiome. Science 328:994–999PubMedCrossRefGoogle Scholar
  28. Nizzoli D, Welsh DT, Fano EA, Viaroli P (2006) Impact of clam and mussel farming on benthic metabolism and nitrogen cycling, with emphasis on nitrate reduction pathways. Mar Ecol Prog Ser 315:151–165CrossRefGoogle Scholar
  29. Rademaker JLW, De Bruijn FJ (1997) Characterization and classification of microbes by REP-PCR genomic fingerprinting and computer-assisted pattern analysis. In: Caetano-Anollés G, Gresshoff PM (eds) DNA markers: protocols, applications and overviews. Wiley, New York, pp 1–26Google Scholar
  30. Rusch A, Huettel M, Reimers CE, Taghon GL, Fuller CM (2003) Activity and distribution of bacterial populations in Middle Atlantic Bight shelf sands. FEMS Microbiol Ecol 44:89–100PubMedCrossRefGoogle Scholar
  31. Rusch DB et al (2007) The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77PubMedCrossRefGoogle Scholar
  32. Santarella-Mellwig R, Franke J, Jaedicke A, Gorjanacz M, Bauer U, Budd A, Mattaj IW, Devos DP (2010) The compartmentalized bacteria of the planctomycetes-verrucomicrobia-chlamydiae superphylum have membrane coat-like proteins. PLoS Biol 8:e1000281PubMedCrossRefGoogle Scholar
  33. Schlesner H (1986) Pirella marina sp. nov., a budding, peptidoglycan-less bacterium from brackish water. Syst Appl Microbiol 8:177–180CrossRefGoogle Scholar
  34. Schlesner H (1994) The development of media suitable for the microorganisms morphologically resembling Planctomyces spp., Pirellula spp., and other Planctomycetales from various aquatic habitats using dilute media. Syst Appl Microbiol 17:135–145CrossRefGoogle Scholar
  35. Schlesner H, Rensmann C, Tindall BJ, Gade D, Rabus R, Pfeiffer S, Hirsch P (2004) Taxonomic heterogeneity within the Planctomycetales as derived by DNA–DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Pirellula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov. and emended description of the genus Pirellula. Int J Syst Evol Microbiol 54:1567–1580PubMedCrossRefGoogle Scholar
  36. Schmidt AS, Bruun MS, Dalsgaard I, Pedersen K, Larsen JL (2000) Occurrence of antimicrobial resistance in fish-pathogenic and environmental bacteria associated with four Danish rainbow trout farms. Appl Environ Microbiol 66:4908–4915PubMedCrossRefGoogle Scholar
  37. Simon J, Kern M, Hermann B, Einsle O, Butt JN (2011) Physiological function and catalytic versatility of bacterial multihaem cytochromes c involved in nitrogen and sulfur cycling. Biochem Soc Trans 39:1864–1870PubMedCrossRefGoogle Scholar
  38. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155Google Scholar
  39. Staley JT (1973) Budding bacteria of the Pasteuria-Blastobacter group. Can J Microbiol 19:609–614PubMedCrossRefGoogle Scholar
  40. Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, Pas-Schoonen KTVD, Webb R, Kuenen JG, Jetten MSM (1999) Missing lithotroph identified as new Planctomycete. Nature 400:446–449PubMedCrossRefGoogle Scholar
  41. Sugita H, Nakamura H, Shimada T (2005) Microbial communities associated with filter materials in recirculating aquaculture systems of freshwater fish. Aquaculture 243:403–409CrossRefGoogle Scholar
  42. Tal Y, Watts JEM, Schreier SB, Sowers KR, Schreier HJ (2003) Characterization of the microbial community and nitrogen transformation processes associated with moving bed bioreactors in a closed recirculated mariculture system. Aquaculture 215:187–202CrossRefGoogle Scholar
  43. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  44. Tendencia EA, de la Peña LD (2001) Antibiotic resistance of bacteria from shrimp ponds. Aquaculture 195:193–204CrossRefGoogle Scholar
  45. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  46. Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831PubMedCrossRefGoogle Scholar
  47. Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17:241–249PubMedCrossRefGoogle Scholar
  48. Ward N, Staley JT, Fuerst JA, Giovannoni S, Schlesner H, Stackebrandt E (2006) The order Planctomycetales, including the genera Planctomyces, Pirellula, Gemmata and Isosphaera and the Candidatus genera Brocadia, Kuenenia and Scalindua. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria. Springer, New York, pp 757–793Google Scholar
  49. Winkelmann N, Harder J (2009) An improved isolation method for attached-living Planctomycetes of the genus Rhodopirellula. J Microbiol Methods 77:276–284PubMedCrossRefGoogle Scholar
  50. Winkelmann N, Jaekel U, Meyer C, Serrano W, Rachel R, Rossello-Mora R, Harder J (2010) Determination of the diversity of Rhodopirellula isolates from European seas by multilocus sequence analysis. Appl Environ Microbiol 76:776–785PubMedCrossRefGoogle Scholar
  51. Zengler K, Toledo G, Rappe M, Elkins J, Mathur EJ, Short JM, Keller M (2002) Cultivating the uncultured. Proc Natl Acad Sci USA 99:15681–15686PubMedCrossRefGoogle Scholar
  52. Zobell CE (1941) Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J Mar Res 4:42–75Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Olga Maria Lage
    • 1
    • 2
  • Joana Bondoso
    • 1
    • 2
  • Flávia Viana
    • 1
  1. 1.Department of Biology, Faculty of SciencesUniversity of PortoPortoPortugal
  2. 2.CIMAR/CIIMAR, Interdisciplinary Centre for Marine and Environmental ResearchUniversity of PortoPortoPortugal

Personalised recommendations