Microbial enzymatic activity and its relation to organic matter abundance on sheltered and exposed beaches on the Polish coast

• Autorzy: Astel A. M. , Bigus K. , Stec M.

Identyfikatory

DOI

10.1016/j.oceano.2018.01.001

• Języki publikacji: EN

Abstrakty

EN

The activity of lipase, aminopeptidase, α-glucosidase, β-glucosidase was correlated and assessed according to an abundance of organic matter and total forms of nutrients in beach sediments characterized by different strength of anthropopressure and degree of sheltering. 76% of the data variance was explained by six factors identified by the use of principal component analysis: (1) anthropogenic rich in N, (2) microbial enzymatic activity, (3) labile organic matter, (4) bacterial growth, (5) anthropogenic rich in P and (6) hydrolytic. Differences in secondary bacterial production according to the distance from the water line, vertical cores and seasonality are limited by the accessibility of biochemical compounds (lipids, proteins, carbohydrates, total organic carbon), total phosphorus and nitrogen. Sediments collected in exposed beaches were not as rich in organic matter as these collected in sheltered ones due to the impact of sea waves of higher energy and backward current facilitating cleaning. The highest microbial enzymatic activity was observed in the beach infilled prior to the tourist season with well-aerated sand mined from the main harbor canal. Microorganisms induce α-glucosidase synthesis to decompose hardly assimilable COM during deficit of easily assimilable PRT and CHO. The lack of easily assimilable matter activates stronger hydrolytic activity in lower layers of core sediments.

Słowa kluczowe

EN

Baltic Sea; coastal sediments; vertical depth; distance from the water line; nutrients; principal component analysis

• Wydawca: Polish Academy of Sciences, Institute of Oceanology ; Elsevier
• Czasopismo: Oceanologia
• Rocznik: 2018
• Tom: No. 60 (3)
• Strony: 312--330
• Opis fizyczny: Bibliogr. 93 poz., rys., tab., wykr.

Twórcy

autor

Astel A. M.

• Faculty of Mathematics and Natural Sciences, Pomeranian University, Słupsk, Poland

autor

Bigus K.

• Faculty of Mathematics and Natural Sciences, Pomeranian University, Słupsk, Poland

autor

Stec M.

• Faculty of Mathematics and Natural Sciences, Pomeranian University, Słupsk, Poland

Bibliografia

• [1] Allen, J. I., Somerfield, P. J., Siddorn, J., 2002. Primary and bacterial production in the Mediterranean Sea: a modeling study. J. Mar. Syst. 33-34, 473-495.
• [2] Antonowicz, J. P., Mudryk, Z., Zdanowicz, M., 2015. A relationship between accumulation of heavy metals and microbiological parameters in the surface microlayer and subsurface water of a coastal Baltic lake. Hydrobiologia 762, 65-80.
• [3] Bartlett, M. S., 1951. The effect of standardization on a chi square approximation in factor analysis. Biometrika 38, 337-344.
• [4] Bednarek, R., Dziadowiec, H., Pokojska, U., Prusinkiewicz, Z., 2005. Research Concerning Ecology and Soil. 344 pp.. PWN, Warsaw, (in Polish).
• [5] Biddanda, B., Riemann, F., 1992. Detrital carbon and nitrogen relations, examined with degrading cellulose. Mar. Ecol. 13 (3), 271-283.
• [6] Bigus, K., Astel, A. M., Niedzielski, P., 2016. Seasonal distribution of metals in vertical and horizontal profiles of sheltered and exposed beaches on Polish coast. Mar. Pollut. Bull. 106 (1-2), 347-359.
• [7] Boetius, A., 1995. Microbial hydrolytic enzyme activities in deep-sea sediments. Helgoländer Meeresuntersuchungen 49, 177-187.
• [8] Brown, A. C., McLachlan, A., 1990. Ecology of Sandy Shores. Elsevier, Amsterdam, 392 pp.
• [9] Buchanan, J. B., Longbottom, M. R., 1970. The determination of organic matter in marine muds: the effect of the presence of coal and the routine determination of proteins. J. Exp. Mar. Biol. Ecol. 5, 158-169.
• [10] Buscail, R., Pocklington, R., Daumas, R., Guidi, L., 1990. Fluxes and budget of organic matter in the benthic boundary layer over the northwestern Mediterranean margin. Cont. Shelf Res. 10, 1089-1122.
• [11] Carney, R. S., 1989. Examining relationship between organic carbon flux and deep-sea deposit feeding. In: Ecology of marine deposit feeders, Lopez, G., Taghon, G., Levinton, J. (Eds.), Lecture Notes on Coastal and Estuarine Studies, vol. 31. Springer, New York, pp. 24-58.
• [12] Cattell, R. B., 1978. The Scientific Use of Factor Analysis in Behavioral and Life Sciences. Plenum Press, New York, 618 pp.
• [13] Cividanes, S., Incera, M., López, J., 2002. Temporal variability in the biochemical composition of sedimentary organic matter in an intertidal flat of the Galician coast (NW Spain). Oceanol. Acta 25, 1-12.
• [14] Danovaro, R., 1996. Detritus-bacteria-meiofauna interactions in a seagrass bed (Posidonia oceanica) of the NW Mediterranean. Mar. Biol. 127, 1-13.
• [15] Danovaro, R., Fabiano, M., Della Croce, N., 1993. Labile organic matter and microbial biomasses in deep-sea sediments (Eastern Mediterranean Sea). Deep-Sea Res. I 40 (5), 953-965.
• [16] Danovaro, R., Marrale, D., Della Croce, N., Parodi, P., Fabiano, M., 1999a. Biochemical composition of sedimentary organic matter and bacterial distribution in the Aegean Sea: trophic state and pelagic-benthic coupling. J. Sea Res. 42, 117-129.
• [17] Danovaro, R., Dinet, A., Duineveld, G., Tselepides, A., 1999b. Benthic response to particulate fluxes in different trophic environments: a comparison between the Gulf of Lions—Catalan sea (W Mediterranean) and the Cretan Sea (E-Mediterranean). Prog. Oceanogr. 44 (1), 287-312.
• [18] Danovaro, R., Dell'Anno, A., Trucco, A., Serresi, M., Vanucci, S., 2001. Determination of virus abundance in marine sediments. Appl. Environ. Microbiol. 67, 1384-1387.
• [19] Daumas, R., Sautriot, D., Calmet, D., 1983. Evolution de constituantslabiles de la matièreorganiquedans les sediments profonds de diversesmargescontinentales. In: D'Orgon à Misedor (Eds.), Géochimieorganique des sédimentsmarins. C.N.R.S, Paris, 99-150.
• [20] Dell'Anno, A., Mei, M. L., Pusceddu, A., Danovaro, R., 2002. Assessing the trophic state and eutrophication of coastal marine systems: a new approach based on the biochemical composition of sediment organic matter. Mar. Pollut. Bull. 44, 611-622.
• [21] DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., Smith, F., 1956. Colorimetric method for determination of sugars and related substances. Anal. Biochem. 28 (3), 350-356.
• [22] Ellery, W. N., Schleyer, M. H., 1984. Comparison of homogenization and ultrasonication as techniques in extracting attached sedimentary bacteria. Mar. Ecol.-Prog. Ser. 15 (3), 247-250.
• [23] Fabiano, M., Danovaro, R., 1994. Composition of organic matter in sediments facing a river estuary (Tyrrhenian Sea): relationships with bacteria and microphytobenthic biomass. Hydrobiologia 277, 71-84.
• [24] Fabiano, M., Danovaro, R., Fraschetti, S., 1995. A three-year time series of elemental and biochemical composition of organic matter in subtidal sediments of the Ligurian Sea (northwestern Mediterranean). Cont. Shelf Res. 15 (11-12), 1453-1469.
• [25] Fabiano, M., Marin, V., Misic, C., Moreno, M., Salvo, V. S., Vezzull, L., 2004. Sedimentary organic matter and bacterial community in microtidal mixed beaches of the ligurian sea (NW Mediterranean). Chem. Ecol. 20 (6), 423-435.
• [26] Fernandes, C. E., Das, A., Nath, B. N., Faria, D. G., LokaBharathi, P. A., 2012. Mixed response in bacterial and biochemical variables to simulated sand mining in placer-rich beach sediments, Ratnagiri, West coast of India. Environ. Monit. Assess. 184 (5), 2677-2689.
• [27] Fichez, R., 1991a. Suspended particulate organic matter in a Mediterranean submarine cave. Mar. Biol. 108, 167-174.
• [28] Fichez, R., 1991b. Composition and fate of organic matter in submarine cave sediments; implications for the biogeochemical cycle of organic carbon. Oceanol. Acta 14 (4), 369-377.
• [29] Forsberg, C., 1991. Eutrophication of the Baltic Sea. Uppsala Univ. Press, Uppsala, 32 pp.
• [30] Fuhrman, J. A., Azam, F., 1982. Thimidine incorporation as a measure of heterotrophic bacterioplankton production in marine Surface waters: evaluation and field results. Mar. Biol. 66 (2), 109-120.
• [31] Germán Rodríguez, J. G., Lastra, M., López, J., 2003. Meiofauna distribution along a gradient of sandy beaches in northern Spain. Estuar. Coast. Shelf Sci. 58, 63-69.
• [32] Graf, G., 1989. Pelagic-benthic coupling in a deep-sea benthic community. Nature 341, 437-439.
• [33] Graf, T. R., Meyer-Reil, L. A., 1985. Remineralization of organic substances on benthic surfaces in the intertidal reef off Mactan, Cebu, Philippines. Phillippine Sci. 22, 42-46.
• [34] Graf, G., Shulz, T., Peinert, R., Meyer-Reil, L. A., 1983. Benthic response to sedimentation events during autumn to spring at a shallow water station in the Western Kiel Bight. I. Analysis of processes on a community level. Mar. Biol. 77 (3), 235-246.
• [35] Grant, J., Hargrave, B. T., 1987. Benthic metabolism and the quality of sediment organic carbon. Biol. Oceanogr. 4 (3), 243-264.
• [36] Håkanson, L., Bryhn, A. C., 2008. Eutrophication in the Baltic Sea: Present Situation, Nutrient Transport Processes, Remedial Strategies. Springer-Verlag, Berlin, 300 pp.
• [37] Halliday, E., Gast, R. J., 2011. Bacteria in beach sands: an emerging challenge in protecting coastal water quality and bather health. Environ. Sci. Technol. 45 (2), 370-379.
• [38] Handa, N., Yanagi, K., Matsunaga, K., 1972. Distribution of detrital material in the Western Ocean and their biochemical nature. Memoriedell'IstitutoItaliano di Idrobiologia 29, 53-71.
• [39] Hervé, A., 2010. Factor Rotations in Factor Analyses, http://www.utd.edu/~herve/Abdi-rotations-pretty.pdf (accessed 17.01.10).
• [40] HELCOM, 2009. Eutrophication in the Baltic Sea — an integrated thematic assessment of the effects of nutrient enrichment and eutrophication in the Baltic Sea region. In: Baltic Sea Environment Proceedings No. 115B, Helsinki Commission. Helsinki 148 pp.
• [41] Heymans, J. J., McLachlan, A., 1996. Carbon budget and network analysis of a high-energy beach/surf-zone ecosystem. Estuar. Coast. Shelf Sci. 43 (4), 485-505.
• [42] Hoppe, H. G., 1984. Relations between bacterial extracellular enzyme activities and heterotrophic substrate uptake in a brackishwater environment. 2. In: Colloque International de Bacteriologie Marine, Brest, France, 1-5.
• [43] Incera, M., Cividanes, M., Lastra, M., López, J., 2003. Temporal and spatial variability of sedimentary organic matter in sandy beaches on the northwest coast of the Iberian Peninsula. Estuar. Coast. Shelf Sci. 58, 55-61.
• [44] Januszkiewicz, T., 1978. Study on methods of chemical analyses of the composition of contemporary bottom sediments in lakes. Olsztyn, Zeszyty Naukowe ART 8, 3-30, (in Polish).
• [45] Jędrzejczak, M. F., 1999. The degradation of stranded carrion on a Baltic Sea sandy beach. Oceanol. Stud. 28 (3-4), 109-141.
• [46] Jugnia, L. B., Tadonléké, R. D., Sime-Ngando, T., Devaux, J., 2000. The microbial food web in the recently flooded Sep Reservoir: diel fluctuations in bacterial biomass and metabolic activity in relations to phytoplankton and flagellate grazers. Microb. Ecol. 40 (4), 317-329.
• [47] Kaiser, E., Herndl, G. J., 1997. Rapid recovery of marine bactrioplankton activity after inhibition by UV radiation in coastal waters. Appl. Environ. Microbiol. 63 (10), 4026-4031.
• [48] Khiyama, H. M., Makemson, J. C., 1973. Sand beach bacteria: enumeration and characterization. Appl. Microbiol. 26 (3), 293-297.
• [49] Khripounoff, A., Crassous, P., Desbrnyères, D., Le Cox, J. R., 1985. Le flux organiqueparticulaire et ses transformations à l'interface eau-sédiment. Oceanol. Acta 8 (3), 293-301.
• [50] Koop, K., Griffiths, C. L., 1982. The relative significance of bacteria, meio- and macrofauna on an exposed sandy beach. Mar. Biol. 66 (3), 295-300.
• [51] Krstulović, N., Solić, M., 1988. Distribution of proteolytic, amylolytic and lipolytic bacteria in the Kastela Bay. Acta Adriat. 29, 75-82.
• [52] Markwell, M. A. K., Hass, S. M., Bieber, L. L., Tolbert, M. E., 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87 (1), 206-210.
• [53] Massart, D. L., Kaufman, L., 1997. The Interpretation of Analytical Chemical Data by the Use of Cluster Analysis. Wiley-Interscience, New York, 237 pp.
• [54] McLachlan, A., De Ruyck, A., Hacking, N., 1996. Community structure on sandy beaches: patterns of richness and zonation in relation to tide range and latitude. Revista Chilena de Historia Natural 69, 451-467.
• [55] Meyer-Reil, L. A., 1983. Benthic response to sedimentation events during autumn to spring at a shallow-water station in the Western Kiel Bight. II. Analysis of benthic bacterial populations. Mar. Biol. 77 (3), 247-256.
• [56] Meyer-Reil, L. A., Bölter, M., Dawson, R., Liebezeit, G., Szwerinski, H., Wolter, K., 1980. Interrelationships between microbiological and chemical parameters of sandy beach sediments, a summer aspect. Appl. Environ. Microbiol. 39 (4), 797-802.
• [57] Misic, C., Fabiano, M., 2005. Enzymatic activity on sandy beaches of the Ligurian Sea (NW Mediterranean). Microb. Ecol. 49 (4), 513-522.
• [58] Mudryk, Z., Podgórska, B., 2006. Enzymatic activity bacterial strains isolated from marine beach. Pol. J. Environ. Stud. 15, 441-448.
• [59] Mudryk, Z., Podgórska, B., 2007. Culturable microorganisms in sandy beaches in the south Baltic Sea. Pol. J. Ecol. 55, 221-231.
• [60] Mudryk, Z., Donderski, W., Skórczewski, P., Walczak, M., 1999. Neustonic and planktonic bacteria isolated from a brackish lake Gardno. Pol. Arch. Hydrobiol. 46, 121-129.
• [61] Mudryk, Z., Skórczewski, P., Perliński, P., Wielgat, M., 2011. Studies concerning heterotrophic bacteria decomposing macromolecular compounds at two marine beaches. Oceanol. Hydrobiol. Stud. 40, 74-83.
• [62] Myślińska, E., 2001. Laboratory Studies of Soils. PWN, Warsaw, 277 pp., (in Polish).
• [63] Nair, S., Loka Bharathi, P. A., 1980. Heterotrophic bacterial population in tropical sandy beaches. Mahasagar 13 (3), 261-267.
• [64] Nordstrom, K. F., 1992. Estuarine Beaches. Elsevier, London/New York, 226 pp.
• [65] Novitsky, J. A., MacSween, M. C., 1989. Microbiology of a high Energy beach sediment: evidence for an active and growing community. Mar. Ecol.-Prog. Ser. 52, 71-75.
• [66] Olańczuk-Neyman, K., Jankowska, K., 1998. Bacteriological investigations of the sandy beach ecosystem in Sopot. Oceanologia 40, 137-151.
• [67] Penna, N., Kovač, N., Ricci, F., Penna, A., Capellacci, S., Faganeli, J., 2009. The role of dissolved carbohydrates in the Northern Adriatic macroaggregate formation. Acta Chim. Slov. 56, 305-314.
• [68] Perliński, P., Mudryk, Z. J., 2016. Activity of extracellular enzymes on the marine beach differing in the level of antropopressure. Environ. Monit. Assess. 188 (3), 188-200.
• [69] Phillips, M. C., Solo-Gabriele, H. M., Reniers, A. J. H. M., Wang, J. D., Kiger, R. T., Abdel-Mottaleb, N., 2011. Pore water transport of enterococci out of beach sediments. Mar. Pollut. Bull. 62 (11), 2293-2298.
• [70] Piggot, A. M., Klaus, J. S., Johnson, S., Phillips, M. C., Solo-Gabriele, H. M., 2012. Relationship between enterococcal levels and sediment biofilms at recreational beaches in South Florida. Appl. Environ. Microbiol. 78 (17), 5973-5982.
• [71] Porter, K. G., Feig, Y. S., 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25 (5), 943-948.
• [72] Report, 2010. The Report on the State of the Environment in the Pomeranian Province in 2010. Biblioteka Monitoringu Środowiska, Gdańsk 169 pp., https://www.gdansk.wios.gov.pl/monitoring/282-raporty-o-stanie-srodowiska-w-wojewodztwie-pomorskim.html (accessed 14.04.16).
• [73] Report, 2012. The Report on the State of the Environment in the Pomeranian Province in 2012. 180 pp.. Biblioteka Monitoringu Środowiska, Gdańsk http://www.gdansk.wios.gov.pl/monitoring/282-raporty-o-stanie-srodowiska-w-wojewodztwie-pomorskim.html (accessed 14.04.16).
• [74] Robinson, J. D., Mann, K. H., Novitsky, J. A., 1982. Conversion of the particulate fraction of seaweed detritus to bacterial biomass. Limnol. Oceanogr. 27 (6), 1072-1079.
• [75] Rodil, I. F., Lastra, M., 2004. Environmental factors affecting benthic macrofauna along a gradient of intermediate sandy beaches in northern Spain. Estuar. Coast. Shelf Sci. 61 (1), 37-44.
• [76] Rodil, L. F., Lastra, M., López, J., 2007. Macroinfauna community structure and biochemical composition of sedimentary organic matter along a gradient of wave exposure in sandy beaches (NW Spain). Hydrobiologia 579 (1), 301-316.
• [77] Rodil, I. F., Cividanes, S., Lastra, M., López, J., 2008. Seasonal variability in the vertical distribution of benthic macrofauna and sedimentary organic matter in an estuarine beach (NW Spain). Estuar. Coasts 31 (2), 382-395.
• [78] Rowe, G. T., Deming, J., 1985. The role of bacteria in the turnover of organic carbon in deep-sea sediments. J. Mar. Res. 43 (4), 925-950.
• [79] Sargent, J. R., Hopkins, C. C. E., Seiring, J. V., Youngson, A., 1983. Partial characterization of organic material in surface sediments from Balsfjorden, northern Norway, in relation to its origin and nutritional value for sediment-ingesting animals. Mar. Biol. 76 (1), 87-94.
• [80] Schoeman, D. S., McLachlan, A., Dugan, J. E., 2000. Lessons from a disturbance experiment in the intertidal zone of an exposed sandy beach. Estuar. Coast. Shelf Sci. 50 (6), 869-884.
• [81] Smayda, T. J., 1997. Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42 (5 Part 2), 1137-1153.
• [82] Szefer, P., 2002. Metals, Metalloids and Radionuclides in the Baltic Sea Ecosystem. Elsevier Science, Amsterdam, 766 pp.
• [83] Thompson, J. K., Nichols, F. H., 1988. Food availability controls seasonal cycle of growth in Macomabalthica (L.) in San Francisco Bay, California. J. Exp. Mar. Biol. Ecol. 116 (1), 43-61.
• [84] Thurstone, L. L., 1947. Multiple Factor Analysis: A Development and Expansion of Vectors of the Mind. University of Chicago Press, Chicago, 535 pp.
• [85] Vandeginste, B. G. M., Massart, D. L., Buydens, L. M. C., De Jong, S., Lewi, P. J., Smeyers-Verbeke, J., 1997. Handbook of Chemometrics and Qualimetrics; Data Handling in Science and Technology, Parts A and B. Elsevier, Amsterdam, 886 pp., 876 pp.
• [86] Vu, N. T., 2016. Algae Biology, https://www.academia.edu/1741106/ALGAE_BIOLOGY (accessed 27.07.16).
• [87] Węsławski, M., Urban-Malinga, B., Kotwicki, L., Opaliński, K. W., Szymelfenig, M., Dutkowski, M., 2000. Sandy coastlines — are there conflicts between recreation and natural values? Oceanol. Stud. 2, 5-18.
• [88] Węsławski, J. M., Szymelfenig, M., Urbański, J., 2005. The Beach: User's Manual. Centre of Excellence for Shelf Seas Science. IO PAN Press, Sopot, 112 pp.
• [89] Wilson, J. O., Buchsbaum, R., Valiela, I., Swain, T., 1986. Decomposition in salt marsh ecosystems: phenolic dynamics during decay of litter of Spartinaalterniflora. Mar. Ecol. Progr. Ser. 29 (2), 177-187.
• [90] Zeng, X., Xiao, X., Wang, F., 2010. Response of bacteria in the deepsea sediments and the Antarctic soils to carbohydrates: effects on ectoenzyme activity and bacterial community. J. Environ. Sci. (China) 22 (11), 1779-1785.
• [91] Ziervogel, K., Mckay, L., Rhodes, B., Osburn, C. L., Dickson-Brown, J., Arnosti, C., Teske, A., 2012. Microbial enzymatic activity and secondary production in sediments affected by the sedimentation pulse following the Deepwater Horizon oil spill. PLoS ONE 7 (4), 34816.
• [92] Ziervogel, K., Joye, S. B., Arnosti, C., 2016. Microbial enzymatic activity and secondary production in sediments affected by the sedimentation pulse following the Deepwater Horizon oil spill. Deep-Sea Res. II 129, 241-248.
• [93] Zöllner, K., Kirsch, A., 1962. Über die quantitative Bestimmung von Lipoiden (Mikromethode) mittels der vielen natürlichen Lipoiden (allen bekannten Plasmalipoiden) gemeinsamen Sulfophosphovanillin-Reaktion. Zeitschriftfür die Gesamte Experimentelle Medizin 135, 545-561.

Uwagi

Opracowanie rekordu w ramach umowy 509/P-DUN/2018 ze środków MNiSW przeznaczonych na działalność upowszechniającą naukę (2018).