Skip to main content

Advertisement

Log in

Bacterial diversity and hydrography of Etoliko, an anoxic semi-enclosed coastal basin in Western Greece

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Etoliko, an anoxic semi-enclosed basin, is part of a complex wetland in Western Greece extremely rich in biodiversity. It covers an area of 1,700 ha with an atypical orientation that has been formed tectonically. In order to identify the main factors influencing the bacterial profile at the Etoliko basin, 48 samples were collected, representing seasonal variation at four sampling stations. Physico-chemical analysis of the samples indicates the presence of three layers in the Etoliko basin: (1) low-density surface layer, (2) a layer with a steep density gradient, and (3) dense water below a depth of 20 m. A permanent halocline, whose thickness is varying seasonally, has been identified in the Etoliko basin water column, while the spatiotemporal salinity distribution was highly affected by the basin’s interaction with the nearby Messolonghi lagoon. The anoxic zone extends from 20 m below the surface to the bottom of the Etoliko basin in summer, while the bottom layer was hypoxic during winter. Bacterial populations were analyzed by Automated Ribosomal Intergenic Spacer Analysis (ARISA). Bacterial richness and diversity were calculated and compared across samples. Hierarchical analysis showed that ARISA clustered the surface water samples according to seasonal variation, while sediment and near-to-bottom water samples appear to be stable and to cluster together. Non-metric multidimensional scaling (MDS) indicates that bacterial composition depends on dissolved oxygen and salinity. Increase in salinity of the ecosystem leads to a significant reduction of the microbial diversity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson MJ (2001) A new method for non parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ (2005) DISTLM v. 5: a FORTRAN computer program to calculate a distance based multivariate analysis for a linear model. Department of Statistics, University of Auckland, New Zealand 10

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA for PRIMER, guide to software and statistical methods. PRIMER E, Plymouth

    Google Scholar 

  • Astor Y, Muller-Karger F, Scranton MI (2003) Seasonal and interannual variation in the hydrography of the Cariaco Basin: implications for basin ventilation. Cont Shelf Res 23(1):125–144

    Article  Google Scholar 

  • Benlloch S, López-López A, Casamayor EO, Øvreås L, Goddard V, Daae FL, Smerdon G, Massana R, Joint I, Thingstad F, Pedros-Alio C, Rodriguez-Valera F (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 4(6):349–360

    Article  PubMed  Google Scholar 

  • Bosshard PP, Santini Y, Grüter D, Stettler R, Bachofen R (2000) Bacterial diversity and community composition in the chemocline of the meromictic alpine lake Cadagno as revealed by 16S rDNA analysis. FEMS Microbiol Ecol 31(2):173–182

    Article  CAS  PubMed  Google Scholar 

  • Boucher D, Jardillier L, Debroas D (2006) Succession of bacterial community composition over two consecutive years in two aquatic systems: a natural lake and a lake-reservoir. FEMS Microbiol Ecol 55(1):79–97

    Article  CAS  PubMed  Google Scholar 

  • Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, Zanardini E, Sorlini C, Corselli C, Daffonchio D (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70(10):6147–6156

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Clement BG, Luther GW, Tebo BM (2009) Rapid, oxygen-dependent microbial Mn(II) oxidation kinetics at sub-micromolar oxygen concentrations in the Black Sea suboxic zone. Geochim Cosmochim Acta 73(7):1878–1889

    Article  CAS  Google Scholar 

  • Dassenakis Μ, Krasakopoulou Ε, Matzara B (1994) Chemical characteristics of Aetoliko lagoon, Greece, after an ecological shock. Mar Pollut Bull 28(7):427–433

    Article  CAS  Google Scholar 

  • Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol 33:245–303

    Google Scholar 

  • Dyrsenn DW (1999) Framvaren and the Black Sea—similarities and differences. Aquat Geochem 5:59–73

    Article  Google Scholar 

  • Fuchsman CA, Kirkpatrick JB, Brazelton WJ, Murray JW, Staley JT (2011) Metabolic strategies of free-living and aggregate-associated bacterial communities inferred from biologic and chemical profiles in the Black Sea suboxic zone. FEMS Microbiol Ecol 78(3):586–603

    Article  CAS  PubMed  Google Scholar 

  • Galand PE, Bourrain M, De Maistre E, Catala P, Desdevises Y, Elifantz H, Kirchman DL, Lebaron P (2012) Phylogenetic and functional diversity of bacteria and archaea in a unique stratified lagoon, the Clipperton atoll (N Pacific). FEMS Microbiol Ecol 79(1):203–217

    Article  CAS  PubMed  Google Scholar 

  • Gianni A, Kehayias G, Zacharias I (2011) Geomorphology modification and its impact to anoxic lagoons. Ecol Eng 37(11):1869–1877

    Article  Google Scholar 

  • Gianni A, Kehayias G, Zacharias I (2012) Temporal and spatial distribution of physicochemical parameters in an anoxic lagoon, Aitoliko, Greece. J Environ Biol 33(1):107–114

    CAS  PubMed  Google Scholar 

  • Giovannoni SJ, Vergin KL (2012) Seasonality in ocean microbial communities. Science 335:671–676

    Google Scholar 

  • Glazer BT, Luther GW III, Konovalov SK, Friederich GE, Trouwborst RE, Romanov AS (2006) Spatial and temporal variability of the Black Sea suboxic zone. Deep-Sea Res II 53:1756–1768

    Article  Google Scholar 

  • Hiscock WT, Millero FJ (2006) Alkalinity of the anoxic waters in the Western Black Sea. Deep-Sea Res II 53:1787–1801

    Article  Google Scholar 

  • Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69(2):1030–1042

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Josefson AB, Hansen JLS (2004) Species richness of benthic macrofauna in Danish estuaries and coastal areas. Glob Ecol Biogeogr 13(3):273–288

    Article  Google Scholar 

  • Josefson AB, Widbom B (1988) Differential response of benthic macrofauna and meiofauna to hypoxia in the Gullmar Fjord basin. Mar Biol 100:31–40

    Article  Google Scholar 

  • Justić D, Legović T, Rottini-Sardini L (1987) Trends in oxygen cintent 1911–1984 and occurrence of benthic mortality in northern Adriatic Sea. Estuar Coast Shelf Sci 25:435–445

    Article  Google Scholar 

  • Justić D, Rabalais NN, Turner RE, Wiseman WJ (1993) Seasonal coupling between riverbone nutrients, net productivity and hypoxia. Mar Pollut Bull 26:184–189

    Article  Google Scholar 

  • Katsaveli K, Vayenas D, Tsiamis G, Bourtzis K (2012). Bacterial diversity in Cr(VI) and Cr(III)-contaminated industrial wastewaters. Extremophiles 16:285–296

    Google Scholar 

  • Kent AD, Yannarell AC, Rusak JA, Triplett EW, McMahon KD (2007) Synchrony in aquaticmicrobial community dynamics. ISME J 1:38–47

    Google Scholar 

  • Konovalov SK, Murray JW, Luther GW III, Tebo BM (2006) Processes controlling the redox budget for the oxic/anoxic water column of the Black Sea. Deep-Sea Res II 53:1817–1841

    Article  Google Scholar 

  • Kuypers MM, Sliekers AO, Lavik G, Schmid M, Jørgensen BB, Kuenen JG, Sinninghe Damsté JS, Strous M, Jetten MS (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422(6932):608–611

    Article  CAS  PubMed  Google Scholar 

  • Lam P, Jensen MM, Lavik G, McGinnis DF, Müller B, Schubert CJ, Amann R et al (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 104(17):7104–7109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Legendre P, Legendre L (2000) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  • Lehours AC, Bardot C, Thenot A, Debroas D, Fonty G (2005) Anaerobic microbial communities in Lake Pavin, a unique meromictic lake in France. Appl Environ Microbiol 71(11):7389–7400

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leonardos I, Trilles JP (2003) Host–parasite relationships: occurrence and effect of the parasitic isopod Mothocya epimerica on sand smelt Atherina boyeri in the Mesolongi and Etolikon Lagoons (W. Greece). Dis Aquat Org 54(3):243–251

    Article  PubMed  Google Scholar 

  • Madrid VM, Taylor GT, Scranton MI, Chistoserdov AY (2001) Phylogenetic diversity of bacterial and archaeal communities in the anoxic zone of the Cariaco Basin. Appl Environ Microbiol 67(4):1663–1674

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mandernack KW, Krouse HR, Skei JM (2003) A stable sulfur and oxygen isotopic investigation of sulfur cycling in an anoxic marine basin, Framvaren Fjord, Norway. Chem Geol 195:181–200

    Article  CAS  Google Scholar 

  • Manske AK, Glaeser J, Kuypers MMM, Overmann J (2005) Physiology and phylogeny of green sulfur bacteria forming a monospecific phototrophic assemblage at a depth of 100 meters in the Black Sea. Appl Environ Microbiol 71(12):8049–8060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Millero FJ (1991) The oxidation of H2S in Framvaren Fjord. Limnol Oceanogr 36:1007–1014

    Article  CAS  Google Scholar 

  • Neretin LN, Volkov II, Böttcher ME, Grinenko VA (2001) A sulfur budget for the Black Sea anoxic zone. Deep-Sea Res I 48:2569–2593

    Article  CAS  Google Scholar 

  • Newton RJ, Mcmahon KD (2011) Seasonal differences in bacterial community composition following nutrient additions in a eutrophic lake. Environ Microbiol 13:887–899

    Article  CAS  PubMed  Google Scholar 

  • Nilsson HC, Rosenberg R (1997) Benthic habitat quality assessment of an oxygen stressed fjord by surface and sediment profile images. J Mar Syst 11:249–264

    Article  Google Scholar 

  • Nixon S (1990) Marine eutrophication: a growing international problem. Ambio 19:101

    Google Scholar 

  • Papadas IT, Katerinopoulos L, Gianni A, Zacharias I, Deligiannakis Y (2009) A theoretical and experimental physicochemical study of sulfur species in the anoxic lagoon of Aitoliko-Greece. Chemosphere 74(8):1011–1017

    Article  CAS  PubMed  Google Scholar 

  • Pedrós-Alió C, Calderón-Paz JI, Gasol JM (2000) Comparative analysis shows that bacterivory, and not viral lysis, controls the abundance of heterotrophic prokaryotic plankton. FEMS Microbiol Ecol 32:157–165

    Article  PubMed  Google Scholar 

  • Percy D, Li X, Taylor GT, Astor Y, Scranton MI (2008) Controls on iron, manganese and intermediate oxidation state sulfur compounds in the Cariaco Basin. Mar Chem 111:47–62

    Article  CAS  Google Scholar 

  • Peura S, Eiler A, Hiltunen M, Nykänen H, Tiirola M, Jones RI (2012) Bacterial and phytoplankton responses to nutrient amendments in a boreal lake differ according to season and to taxonomic resolution. PLoS ONE 7(6):e38552

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pinhassi J, Hagström Å (2000) Seasonal succession in marine bacterioplankton. Aquat Microb Ecol 21(3):245–256

    Article  Google Scholar 

  • Powilleit M, Kube J (1999) Effects of severe oxygen depletion on macrobenthos in the Pomeranian Bay (southern Baltic Sea): a case study in a shallow, sublittoral habitat characterised by low species richness. J Sea Res 42:221–234

    Article  Google Scholar 

  • Schauer M, Balagué V, Pedrós-Alió C, Massana R (2003) Seasonal changes in the taxonomic composition of bacterioplankton in a coastal oligotrophic system. Aquat Microb Ecol 31(2):163–174

    Article  Google Scholar 

  • Vetriani C, Tran HV, Kerkhof LJ (2003) Fingerprinting microbial assemblages from the oxic/anoxic chemocline of the Black Sea. Appl Environ Microbiol 69(11):6481–6488

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu RSS (1999) Eutrophication, trace organics and water-borne pathogens: pressing problems and challenge. Mar Pollut Bull 39:11–22

    Article  CAS  Google Scholar 

  • Yannarell AC, Kent AD, Lauster GH, Kratz TK, Triplett EW (2003) Temporal patterns in bacterial communities in three temperate lakes of different trophic status. Microb Ecol 46(4):391–405

    Article  CAS  PubMed  Google Scholar 

  • Yao W, Millero FJ (1995) The chemistry of the anoxic waters in the Framvaren Fjord, Norway. Aquat Geochem 1:53–88

    Article  CAS  Google Scholar 

  • Yemenicioglu S, Erdogan S, Tugrul S (2006) Distribution of dissolved forms of iron and manganese in the Black Sea. Deep-Sea Res II 53:1842–1855

    Article  CAS  Google Scholar 

  • Zwart G, Crump BC, Agterveld M, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available16S rRNA gene sequences from plankton of lakes andrivers. Aquat Microb Ecol 28:141–155

    Google Scholar 

  • Zwisler W, Selje N, Simon M (2003) Seasonal patterns of the bacterioplankton community composition in a large mesotrophic lake. Aquat Microb Ecol 31(3):211–225

    Article  Google Scholar 

Download references

Acknowledgments

This work was partially supported by EU CSA-REGPROT 203590 – MicrobeGR and by EU PEOPLE-2012-IAPP 324349.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to George Tsiamis or Kostas Bourtzis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chamalaki, A., Gianni, A., Kehayias, G. et al. Bacterial diversity and hydrography of Etoliko, an anoxic semi-enclosed coastal basin in Western Greece. Ann Microbiol 64, 661–670 (2014). https://doi.org/10.1007/s13213-013-0700-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-013-0700-3

Keywords

Navigation