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.
Similar content being viewed by others
References
Bengtsson MM, Ovreas L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:261
Bengtsson MM, Sjøtun K, Øvreås L (2010) Seasonal dynamics of bacterial biofilms on the kelp Laminaria hyperborea. Aquat Microb Ecol 60:71–83
Bissett A, Bowman J, Burke C (2006) Bacterial diversity in organically-enriched fish farm sediments. FEMS Microbiol Ecol 55:48–56
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 219:83–97
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 55:857–871
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 21:73–84
Cohen-Bazire G, Sistrom WR, Stanier RY (1957) Kinetic studies of pigment synthesis by non-sulphur purple bacteria. J Cell Comp Physiol 49:25–68
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 71:6134–6141
DeLong EF, Franks DG, Alldredge L (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934
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 119–144
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
Gade D, Gobom J, Rabus R (2005a) Proteomic analysis of carbohydrate catabolism and regulation in the marine bacterium Rhodopirellula baltica. Proteomics 5:3672–3683
Gade D, Stührmann T, Reinhardt R, Rabus R (2005b) Growth phase dependent regulation of protein composition in Rhodopirellula baltica. Environ Microbiol 7:1074–1084
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 1–11
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 100:8298–8303
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 12:719–727
Kawahara N, Shigematsu K, Miyadai T, Kondo R (2009) Comparison of bacterial communities in fish farm sediments along an organic enrichment gradient. Aquaculture 287:107–113
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 10:1260–1270
Kummerer K (2009) Antibiotics in the aquatic environment—a review—part I. Chemosphere 75:417–434
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 13:655–665
Lage OM, Bondoso J (2011) Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 78:366–375
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175
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 107:12883–12888
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 107:1935–1946
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 49:433–443
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 29:333–348
Nelson KE et al (2010) A catalog of reference genomes from the human microbiome. Science 328:994–999
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 315:151–165
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 1–26
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 44:89–100
Rusch DB et al (2007) The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77
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:e1000281
Schlesner H (1986) Pirella marina sp. nov., a budding, peptidoglycan-less bacterium from brackish water. Syst Appl Microbiol 8:177–180
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 17:135–145
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 54:1567–1580
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 66:4908–4915
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 39:1864–1870
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155
Staley JT (1973) Budding bacteria of the Pasteuria-Blastobacter group. Can J Microbiol 19:609–614
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 400:446–449
Sugita H, Nakamura H, Shimada T (2005) Microbial communities associated with filter materials in recirculating aquaculture systems of freshwater fish. Aquaculture 243:403–409
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 215:187–202
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tendencia EA, de la Peña LD (2001) Antibiotic resistance of bacteria from shrimp ponds. Aquaculture 195:193–204
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 22:4673–4680
Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831
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
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 757–793
Winkelmann N, Harder J (2009) An improved isolation method for attached-living Planctomycetes of the genus Rhodopirellula. J Microbiol Methods 77:276–284
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 76:776–785
Zengler K, Toledo G, Rappe M, Elkins J, Mathur EJ, Short JM, Keller M (2002) Cultivating the uncultured. Proc Natl Acad Sci USA 99:15681–15686
Zobell CE (1941) Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J Mar Res 4:42–75
Acknowledgments
We would like to thank Fernando Tavares for phylogenetic support, Helena Abreu and Rui Pereira for sample collection and Rogério Tenreiro (BioFig) for the utilization of the BioNumerics and interpretation of data. This study was financially supported by the pluriannual program of Fundação para a Ciência e Tecnologia (FCT).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Erko Stackebrandt.
Rights and permissions
About this article
Cite this article
Lage, O.M., Bondoso, J. & Viana, F. Isolation and characterization of Planctomycetes from the sediments of a fish farm wastewater treatment tank. Arch Microbiol 194, 879–885 (2012). https://doi.org/10.1007/s00203-012-0821-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-012-0821-2