Abstract
Kandalaksha Bay is an estuarine system located around the North Polar Circle in the White Sea (Russia). This peculiar environment, showing big sea level differences during tide cycles causing intense water mixing, is almost unknown concerning its microbial diversity. In this work, seawater bacterial communities, mainly obtained from a coastal area, were studied in order to gather information on their structure and most abundant populations. The study was carried out by cluster analysis of polymerase chain reaction–temperature-gradient gel electrophoresis (PCR-TGGE) fingerprinting of partial 16S-rRNA gene amplicons. Bacterial communities were strongly homogenized by tidal water mixing, especially on surface layers and close to the shore. Samples collected from the intertidal zone and the nearby sea surface grouped together with a high percentage of similarity, while those taken offshore at various depths showed evident differences. Multivariate analysis indicated depth as the most significant environmental parameter causing variations in the community structure. High levels of diversity were revealed by both the Simpson’s index of diversity and the range-weighted richness index. The functional organization index suggested that the community was potentially able to preserve its functionality under stressing environmental perturbations. Sequencing of TGGE bands showed that most of the bacteria populations were evolutionarily close to α-proteobacteria. Some γ-proteobacteria and Actinobacteria were revealed too. This work represents the first major contribution to understanding bacterial diversity in Kandalaksha Bay.
Similar content being viewed by others
References
Allison D, Martiny BH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci 105:11512–11519
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
Arahal D, Ventosa A (2006) The family Halomonadaceae. 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 811–835
Arahal DR, Castillo AM, Ludwig W, Schleifer KH, Ventosa A (2002) Proposal of Cobetia marina gen. nov., comb. nov., within the Family Halomonadaceae, to include the species Halomonas marina. Syst Appl Microbiol 25:207–211
Bent SJ, Forney LJ (2008) The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J 2:689–695
Berger VY, Gorbushin AM (2001) Tolerance and resistance in gastropod mollusks Hydrobia ulvae and H. ventrosa from the White Sea to abiotic environmental factors. Russ J Mar Biol 27:314–319
Brinkhoff T, Giebel HA, Simon M (2008) Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189:531–539
Buchan A, González JM, Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71:5665–5677
Dolotov Y, Filatov N, Shevchenko V, Nemova N, Rimskii-Korsakov N, Denisenko N, Kutcheva I, Boyarinov P, Petrov M, Lifshitz V, Platonov A, Demina L, Kukharev V, Kovalenko V, Zdorovennov R, Rat’kova T, Sergeeva O, Novigatskii A, Pautova L, Filipieva K, Nothig EM, Loronzen C (2005) Monitoring tidal conditions in estuaries of the Karelian Coast of the White Sea. Water Res 32:611–628
Federici E, Giubilei MA, Santi G, Zanaroli G, Negroni A, Fava F, Petruccioli M, D’Annibale A (2012) Bioaugmentation of a historically contaminated soil by polychlorinated biphenyls with Lentinus tigrinus. Microb Cell Factories 11:35
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the Bootstrap. Evolution 39:783–791
Felske A, Wolterink A, Van Lis R, De Vos WM, Akkermans ADL (1999) Searching for predominant soil bacteria: 16S rDNA cloning versus strain cultivation. FEMS Microbiol Ecol 30:137–145
Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436
Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S (2006) Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci 103:13104–13109
Gómez-Silván C, Molina-Muñoz M, Poyatos JM, Ramos A, Hontoria E, Rodelas B, González-López J (2010) Structure of archaeal communities in membrane-bioreactor and submerged-biofilter wastewater treatment plants. Bioresour Technol 101:2096–2105
Howland RJM, Pantiulin AN, Millward GE, Prego R (1999) The hydrography of the Chupa Estuary, White Sea, Russia. Estuar Coast Shelf Sci 48:1–12
Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774
Ivanova EP, Christen R, Sawabe T, Alexeeva YV, Lysenko AM, Chelomin VP, Mikhailov VV (2005) Presence of ecophysiologically diverse populations within Cobetia marina strains isolated from marine invertebrate, algae and the environments. Microbes Environ 20:200–207
Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405
Kaye JZ, Márquez MC, Ventosa A, Baross JA (2004) Halomonas neptunia sp. nov., Halomonas sulfidaeris sp. nov., Halomonas axialensis sp. nov. and Halomonas hydrothermalis sp. nov.: halophilic bacteria isolated from deep-sea hydrothermal-vent environments. Int J Syst Evol Microbiol 54:499–511
Kravchishina M, Mitzkevich I, Veslopolova E, Shevchenko V, Lisitzin A (2008) Relationship between the suspended particulate matter and microorganisms in the White Sea waters. Oceanology 48:837–854
Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306
Labrenz M, Lawson P, Tindall B, Collins M, Hirsch P (2005) Roseisalinus antarcticus gen. nov., sp. nov., a novel aerobic bacteriochlorophyll a-producing a-proteobacterium isolated from hypersaline Ekho Lake, Antarctica. Int J Syst Evol Microbiol 55:41–47
Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge
Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56
Martínez-Checa F, Béjar V, Martínez-Cánovas MJ, Llamas I, Quesada E (2005) Halomonas almeriensis sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium from Cabo de Gata, Almería, south-east Spain. Int J Syst Evol Microbiol 55:2007–2011
Marzorati M, Wittebolle L, Boon N, Daffonchio D, Verstraete W (2008) How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol 10:1571–1581
Maza-Marquez P, Martinez-Toledo MV, Gonzalez-Lopez J, Rodelas B, Juarez-Jimenez B, Fenice M (2013) Biodegradation of olive washing wastewater pollutants by highly efficient phenol-degrading strains selected from adapted bacterial community. Int Biodeterior Biodegrad 82:192–198
Melnikov IA, Korneeva GA, Zhitina LS, Shanin SS (2003) Dynamics of ecological–biochemical characteristics of sea ice in coastal waters of the White Sea. Biol Bull 30:164–171
Munn CB (2011) Marine microbiology: Ecology and applications. Garland Science, New York
Muyzer G (1999) DGGE/TGGE a method for identifying genes from natural ecosystems. Curr Opin Microbiol 2:317–322
Muyzer G, Ramsing NB (1995) Molecular methods to study the organization of microbial communities. Water Sci Technol 32:1–9
Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek J Microb 73:127–141
Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Nicolaisen MH, Ramsing NB (2002) Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J Microbiol Meth 50:189–203
Overland JE, Wood KR, Wang M (2011) Warm Arctic cold continents: climate impacts of the newly open Arctic Sea. Polar Res. doi:10.3402/polar.v30i0.15787
Pantyulin AN (1990) On the formation and variability of the water structure in the White Sea. In: Matekin PV (ed) Biologicheskie resursy Belogo morya (Biological Resources of the White Sea). Moscow State University, Moscow, pp 9–16
Pantyulin AN (2003) Hydrological system of the White Sea. Oceanology 43(suppl 1):S1–S14
Pesciaroli C, Cupini F, Selbmann L, Barghini P, Fenice M (2012) Temperature preferences of bacteria isolated from seawater collected in Kandalaksha Bay, White Sea, Russia. Polar Biol 35:435–445
Pommier T, Canbäck B, Riemann L, Boström KH, Simu K, Lundberg P, Tunlid A, Hagström Å (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16:867–880
Ranjard L, Poly F, Nazaret S (2000) Monitoring complex bacterial communities using culture-independent molecular techniques: application to soil environment. Res Microbiol 151:167–177
Reboleiro-Rivas P, Juarez-Jimenez B, Martinez-Toledo MV, Rodelas B, Andrade L, Gonzalez-Lopez J, Fenice M (2013) Bacterial communities’ structure in a high mountain lake during the ice-free season: cultural and PCR-TGGE investigations. Int J Environ Res 7:685–696
Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Savvichev AS, Rusanov II, Yusupov SK, Bairamov IT, Pimenov NV, Lein AY, Ivanov MV (2003) The process of microbial sulfate reduction in sediments of the coastal zone and littoral of the Kandalaksha Bay of the White Sea. Microbiology 72:478–489
Savvichev AS, Rusanov II, Yusupov SK, Pimenov NV, Lein AY, Ivanov MV (2004) The biogeochemical cycle of methane in the coastal zone and littoral of the Kandalaksha Bay of the White Sea. Microbiology 73:457–468
Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596
Simpson EH (1949) Measurement of diversity. Nature 163:688
Sokal RR, Rohlf F (1962) The comparison of dendrograms by objective methods. Taxon 11:33–40
Spring S, Schulze R, Overmann J, Schleifer KH (2000) Identification and characterization of ecologically significant prokaryotes in the sediment of freshwater lakes: molecular and cultivation studies. FEMS Microbiol Rev 24:573–590
Sumich JL, Morrissey J (2004) Introduction to the biology of marine life. Jones and Bartlett Learning, Sudbury
Tocchi C, Federici E, Fidati L, Manzi R, Vinciguerra V, Petruccioli M (2012) Aerobic treatment of dairy wastewater in an industrial three-reactor plant: effect of aeration regime on performances and on protozoan and bacterial communities. Water Res 46:3334–3344
Vílchez R, Pozo C, Gómez MA, Rodelas B, González-López J (2007) Dominance of sphingomonads in a copper-exposed biofilm community for groundwater treatment. Microbiology 153:325–337
Wagner M, Amann R, Lemmer H, Schleifer KH (1993) Probing activated sludge with oligonucleotides specific for proteobacteria: inadequacy of culture-dependent methods for describing microbial community structure. Appl Environ Microbiol 59:1520–1525
Wagner-Döbler I, Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60:255–280
Ward BB, O’Mullan GD (2002) Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing γ − proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl Environ Microbiol 68:4153–4157
Webster NS, Wilson KJ, Blackall LL, Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
Yumoto I, Hirota K, Iwata H, Akutsu M, Kusumoto K, Morita N, Ezura Y, Okuyama H, Matsuyama H (2004) Temperature and nutrient availability control growth rate and fatty acid composition of facultatively psychrophilic Cobetia marina strain L-2. Arch Microbiol 181:345–351
Zhao X, Yang L, Yu Z, Peng N, Xiao L, Yin D, Qin B (2008) Characterization of depth-related microbial communities in lake sediment by denaturing gradient gel electrophoresis of amplified 16S rRNA fragments. J Environ Sci 20:224–230
Acknowledgments
The authors wish to thank Prof. A. Tzetlin and Dr. A. Zhadan, Department of Biology, Lomonosov Moscow State University, for their kind support during the sampling campaign carried out at the “White Sea Biological Station”, Kandalaksha Bay, Russia. The research was partially financed by the Italian-Russian Institute of Ecological Formation and Research (IIRFRE, Istituto Italo-Russo di Formazione e Ricerche Ecologiche). The Instituto de Parasitología y Biología Molecular Lopez Neyra (CSIC, Granada) is also acknowledged for their DNA sequencing service.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pesciaroli, C., Rodelas, B., Juarez-Jiménez, B. et al. Bacterial community structure of a coastal area in Kandalaksha Bay, White Sea, Russia: possible relation to tidal hydrodynamics. Ann Microbiol 65, 443–453 (2015). https://doi.org/10.1007/s13213-014-0877-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-014-0877-0