Abstract
The abundance of culturable heterotropic bacteria studied on and according to depth levels and seasons in the Gulf of Antalya. Environmental factors were compared regarding culturable heterotrophic bacteria abundance and diversities of bacteria. During the study period (between August 2009 and April 2010, seasonally in the Gulf of Antalya, at six stations and six depth levels (0–20 cm, 10, 25, 50, 100, 200 m). The bacterial isolates were identified in the automated micro identification system VITEK 2 Compact 30 (Biomereux, France). The mean abundance was higher in Sts. D, E and F than Sts. A, B and C, located in the eastern part of the gulf. The mean abundance decreased as the depth level increased. The mean abundance of CHB ranged between 8.15 × 106 and 2.54 × 108 CFU ml−1 throughout the year. Abundance of CHB differed according to the variations of biotic and abiotic factors. A total of 27 taxa of bacteria including six bacterial classes were reported in this study as the first records for the Gulf of Antalya. Six bacterial classes: Gamma Proteobacteria (46.81 %), Bacilli (27.66 %), Beta Proteobacteria (12.77 %), Alfa Proteobacteria (6.38 %), Actinobacteria (4.26 %) and Flavobacteria (2.13 %) were determined. The study resulted in increased knowledge on the composition and biochemical response of bacteria isolated from eutrophic and oligotrophic areas. 23 bacteria species belonging to 16 families were reported.
Similar content being viewed by others
References
Albertelli G, Covazzi-Harriague A, Danovaro R, Fabiano M, Fraschetti S, Pusceddu A (1999) Differential responses of bacteria, meiofauna and macrofauna in a shelf area (Ligurian Sea, NW Mediterranean): role of food availability. J Sea Res 42:11–26. doi:10.1016/S1385-1101(99)00012-X
Allen AE, Howard-Jones MH, Booth MG, Frischer ME, Verity PG, Bronk DA, Sanderson MP (2002) Importance of heterotrophic bacterial assimilation of ammonium and nitrate in the Barents Sea during summer. J Mar Syst 38:93–108. doi:10.1016/S0924-7963(02)00171-9
Altug G, Balkis N (2009) Levels of some toxic elements and frequency of bacterial heavy metal resistance in sediment and sea water. Environ Monit Assess 149:61–69. doi:10.1007/s10661-008-0183-z
Altuğ G et al (2011) Biodiversity of the northern Aegean Sea and southern part of the Sea of Marmara. Mar Biodivers Rec, Turkey. doi:10.1017/S1755267211000662
Anderson M, Ter Braak C (2003) Permutational tests for multi-factorial analysis of variance. J Stat Comput Simul 73:85–113
APHA (1999) Standard methods for the examination of water and waste water, 20th edn. American Public Health Association, Washington
Araujo RM, Arribas RM, Pares R (1991) Distribution of Aeromonas species in waters with different levels of pollution. J Appl Bacteriol 71:182–186. doi:10.1111/j.1365-2672.1991.tb02976.x
Atik M, Ortaçeşme V, Erdoğan R (2011) Natural Environment and Culture in the Mediterranean Region II vol 15. Landscape Diversity in the Mediterranean Region of Turkey. Cambridge Scholars Publishing in association with GSE Research. doi:10.5848/CSP.3107.00010
Azam FT, Fenchel JG, Field JS, Gray LA, Meyer-Reil FT (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
Azov Y (1991) Eastern Mediterranean marine desert? Mar Pollut Bull 23:225–232. doi:10.1016/0025-326X(91)90679-M
Caroppo C, Stabili L, Cavallo RA (2003) Diatoms and bacteria diversity: study of their relationships in the Southern Adriatic Sea Mediterranean Marine. Science 4:73–82
Cavallo RA, Rizzi C, Vozza T, Stabili L (1999) Viable heterotrophic bacteria in water and sediment in “Mar Piccolo” of Taranto’ (Ionian Sea, Italy). J Appl Microbiol 86:906–916
Coma R, Ribes M, Gili J-M, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453. doi:10.1016/S0169-5347(00)01970-4
Danovaro R, Croce ND, Eleftheriou A, Fabiano M, Papadopoulou N, Smith C, Tselepides A (1995) Meiofauna of the deep Eastern Mediterranean Sea: distribution and abundance in relation to bacterial biomass, organic matter composition and other environmental factors. Prog Oceanogr 36:329–341. doi:10.1016/0079-6611(96)00002-X
Danovaro R, Dell’Anno A, Fabiano M, Pusceddu A, Tselepides A (2001) Deep-sea ecosystem response to climate changes: the eastern Mediterranean case study. Trends Ecol Evol 16:505–510. doi:10.1016/S0169-5347(01)02215-7
DeLong EF, Franks DG, Alldredge AL (1993) Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages. Limnol Oceanogr 38:924–934
Duarte CM (2000) Marine biodiversity and ecosystem services: an elusive link. J Exp Mar Biol Ecol 250:117–131. doi:10.1016/S0022-0981(00)00194-5
Ducklow HW, Carlson CA, Bates NR, Knap AH, Michaels AF (1995) Dissolved organic carbon as a component of the biological pump in the North Atlantic Ocean. Soc Sci Ser 348:161–167
Ediger D, Tuğrul S, Yılmaz A (2005) Vertical profiles of particulate organic matter and its relationship with chlorophyll-a in the upper layer of the NE Mediterranean Sea. J Mar Syst 55:311–326. doi:10.1016/j.jmarsys.2004.09.003
EPA(US Environmental Protection Agency) (2007) Ambient water quality criteria for bacteria-1986. US Environmental Protection Agency, EPA-440/5-84-002, Washington, DC
Fong P, Zedler JB (1993) Temperature and light effects on the seasonal succession of algal communities in shallow coastal lagoons. J Exp Mar Biol Ecol 171:259–272
Fuhrman JA, McCallum K, Davis AA (1993) Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans. Appl Environ Microbiol 59:1294–1302
Giovannoni S, Rappé M (2000) Evolution, diversity and molecular ecology of marine prokaryotes. Microbial ecology of the ocean. Wiley-Liss, New York
Gurun S, Kımıran-Erdem A (2013) Examination of the level of bacteriological pollution in the discharge area of the Ayamama Stream to the Marmara Sea. Ekoloji 22:48–57
Hagstrom A, Pommier T, Rohwer F, Simu K, Stolte W, Svensson D, Zweifel U (2002) Use of 16S ribosomal DNA for delineation of marine bacterioplankton species. Appl Environ Microbiol 68:3628–3633. doi:10.1128/AEM.68.7.3628-3633.2002
Henneke E, De Lange GJ (1990) The distribution of DOC and POC in the water column and brines of the Tyro and Bannock Basins. Mar Chem 31:113–122. doi:10.1016/0304-4203(90)90033-9
Hitchins AD, Feng P, Watkins WD, Ripley SR, Chandler LA (1992) Escherichia coli and the coliforms. Bacteriological Analytical Manual, 7th edn. APHA, Washington, DC
Holt R, Lawton J (1994) The ecological consequences of shared natural enemies vol 25. Annu Rev Ecol Syst. Annual Reviews Inc., 4139 El Camino Way, PO Box 10139, Palo Alto, CA 94303-0139. doi:10.1146/annurev.es.25.110194.002431
Hopkins DW, Sparrow AD, Elberling B, Gregorich EG, Novis PM, Greenfield LG, Tilston EL (2006) Carbon, nitrogen and temperature controls on microbial activity in soils from an Antarctic dry valley. Soil Biol Biochem 38:3110–3140. doi:10.1016/j.soilbio.2006.01.012
ICES (1995) Report on the results of the fifth ICES intercomparison exercise for nutrients in sea water. International Council for the Exploration of the Sea, Copenhagen
Jorgensen B, Des Marais D (1988) Optical properties of benthic photosynthetic communities: fiber-optic studies of cyanobacterial mats. Limnol Oceanogr 33:99–113
Jürgens K, Güde H (1994) The potential importance of grazing-resistant bacteria in planktonic systems. Mar Ecol Prog 112:169–188
Kalantzi I, Shimmield TM, Pergantis SA, Papageorgiou N, Black KD, Karakassis I (2013) Heavy metals, trace elements and sediment geochemistry at four Mediterranean fish farms. Sci Tot Environ 444:128–137. doi:10.1016/j.scitotenv.2012.11.082
Kirchman DL, Keel RG, Simon M, Welschmeyer NA (1993) Biomass and production of heterotrophic bacterioplankton in the oceanic subarctic Pacific. Deep Sea Res Part I Oceanogr Res Pap 40:967–988. doi:10.1016/0967-0637(93)90084-G
Krom MD, Kress N, Brenner S, Gordon LI (1991) Phosphorus limitation of primary productivity in the eastern Mediterranean Sea. Limnol Oceanogr 36:424–432
Landa M et al (2013) Phylogenetic and structural response of heterotrophic bacteria to dissolved organic matter of different chemical composition in a continuous culture study. Environ Microbiol. doi:10.1111/1462-2920.12242
Landa M et al (2014) Phylogenetic and structural response of heterotrophic bacteria to dissolved organic matter of different chemical composition in a continuous culture study. Environ Microbiol 16:1668–1681. doi:10.1111/1462-2920.12242
Madigan MT, Martınko JM, Dunlap PV, Clark DP (2009) Brock biology of microorganisms, 12th edn. Pearson Benjamin Cummings, San Francisco
Martin YP, Bianchi MA (1980) Structure, diversity, and catabolic potentialities of aerobic heterotrophic bacterial populations associated with continuous cultures of natural marine phytoplankton. Microb Ecol 5:265–279. doi:10.1007/bf02020334
Martin P, Dyhrman ST, Lomas MW, Poulton NJ, Van Mooy BAS (2014) Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus. Proc Natl Acad Sci USA 111:8089–8094. doi:10.1073/pnas.1321719111
Morrissey EM, Gillespie JL, Morina JC, Franklin RB (2014) Salinity affects microbial activity and soil organic matter content in tidal wetlands. Glob Change Biol 20:1351–1362. doi:10.1111/gcb.12431
Naeem M, Idrees M, Khan MMA, Moinuddin, Ansari AA (2014) Task of mineral nutrients in eutrophication. In: Ansari AA, Gill SS (eds) Eutrophication: causes, consequences and control. Springer, Netherlands, pp 223–237. doi:10.1007/978-94-007-7814-6_16
Neill M (2004) Microbiological Indices for total coliform and E. coli bacteria in estuarine waters. Mar Pollut Bull 49:752–760. doi:10.1016/j.marpolbul.2004.05.016
Parsons T, Maita Y, Lalli C (1984) A manual of chemical and biological methods for seawater analysis. Pergamon, Oxford
Pomeroy LR, Don D (1980) Aggregation of organic matter by pelagic tunicates. Limnol Oceanogr 25:643–652. doi:10.4319/lo.1980.25.4.0643
Reynolds CS (1984) The ecology of freshwater phytoplankton. Cambridge University Press, Cambridge
Riemann L, Middelboe M (2002) Viral lysis of marine bacterioplankton: implications for organic matter cycling and bacterial clonal composition. Ophelia 56:57–68. doi:10.1080/00785236.2002.10409490
Sanders R, Caron D, Berninger U (1992) Relationships between bactena and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem compansion. Mar Ecol Prog 86:1–14
Stabili L, Cavallo RA (2011) Microbial pollution indicators and culturable heterotrophic bacteria in a Mediterranean area (Southern Adriatic Sea Italian coasts). J Sea Res 65:461–469
Stecchini ML, Domenis C (1994) Incidence of Aeromonas species in influent and effluent of urban wastewater purification plants. Lett Appl Microbiol 19:237–239. doi:10.1111/j.1472-765X.1994.tb00952.x
Teira E, Gasol JM, Aranguren-Gassis M, Fernández A, González J, Lekunberri I, Álvarez-Salgado XA (2008) Linkages between bacterioplankton community composition, heterotrophic carbon cycling and environmental conditions in a highly dynamic coastal ecosystem. Environ Microbiol 10:906–917. doi:10.1111/j.1462-2920.2007.01509.x
Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge
Varela M, Bode A, Morán X, Valencia J (2006) Dissolved organic nitrogen release and bacterial activity in the upper layers of the Atlantic Ocean. Microb Ecol 51:487–500. doi:10.1007/s00248-006-9054-8
Wiebe W, Sheldon J, Wade M, Pomeroy J, Lawrence R (1993) Evidence for an enhanced substrate requirement by marine mesophilic bacterial isolates at minimal growth temperatures. Microb Ecol 25:151–159. doi:10.1007/bf00177192
Zenetos A, Siokou-frangou I, Gotsis-Skretas O (2002) The Mediterranean Sea—blue oxygen-rich, nutrient-poor waters. European Environment Agency, Copenhagen
Acknowledgments
We would like to thank Prof. Dr. Gülşen Altuğ and Assoc. Prof. Dr. Umur Onal for their valuable comments and support, and Captain Akın Akyar and the crew of the “Akyarlar” for their help in collecting the samples.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Çardak, M., Özgür Özbek, E. & Kebapçioğlu, T. Seasonal abundance and diversity of culturable heterotrophic bacteria in relation to environmental factors in the Gulf of Antalya, Eastern Mediterranean, Turkey. World J Microbiol Biotechnol 31, 569–582 (2015). https://doi.org/10.1007/s11274-015-1810-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-015-1810-9