Penicillin-mediated changes in viable benthic diatom assemblages – insights about the relevance of bacteria across spatial and seasonal scales
Priya M. D’Costa A and Arga C. Anil A BA CSIR-National Institute of Oceanography, Dona Paula 403004, Goa, India.
B Corresponding author. Email: acanil@nio.org
Marine and Freshwater Research 65(5) 437-452 https://doi.org/10.1071/MF13083
Submitted: 2 April 2013 Accepted: 20 September 2013 Published: 18 December 2013
Abstract
Penicillin, a β-lactam antibiotic, cannot affect diatoms directly but does so through bacteria. Its effects on viable benthic diatom assemblages in a tropical environment were evaluated across spatial (intertidal sandflat, mangrove site, port environment) and seasonal (post-monsoon, pre-monsoon, monsoon) scales. Penicillin treatment resulted in bacterial suppression and a reduction in diatoms at the intertidal and mangrove sites having stable pennate-dominated assemblages. Diatom response at the port site, dominated by transient centric diatoms, ranged from total inhibition to enhancement. The monsoon diatom assemblages, which differed in composition from those in other seasons, showed reduced susceptibility to penicillin. These observations highlight the bacterial influence on diatom assemblages and the significance of species composition of diatom assemblages in these interactions. Epipsammic diatoms (Cocconeis, Grammatophora and Thalassionema) were more sensitive to penicillin than epipelic forms, probably due to: (1) their inability to escape unfavourable bacterial metabolites because of limited diffusion in benthic environments; and (2) the interference of penicillin with the bacterial ‘conditioning’ film required for their attachment. Overall, the observations from the present, preliminary, ecological study provide insights into the relevance of bacteria in influencing viable benthic diatom assemblages across spatial and seasonal scales and emphasise the need for future mesocosm experiments on these aspects.
Additional keywords: bacteria, benthic diatoms, epipelic, epipsammic, monsoon, penicillin.
References
Amin, S. A., Parker, M. S., and Armbrust, E. V. (2012). Interactions between diatoms and bacteria. Microbiology and Molecular Biology Reviews 76, 667–684.| Interactions between diatoms and bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFSjtb3P&md5=5effc94f3c5446733fc47a5a7194737bCAS | 22933565PubMed |
Barranguet, C., Kromkamp, J., and Peene, J. (1998). Factors controlling primary production and photosynthetic characteristics of intertidal microphytobenthos. Marine Ecology Progress Series 173, 117–126.
| Factors controlling primary production and photosynthetic characteristics of intertidal microphytobenthos.Crossref | GoogleScholarGoogle Scholar |
Bruckner, C. G., Bahulikar, R., Rahalkar, M., Schink, B., and Kroth, P. G. (2008). Bacteria associated with benthic diatoms from Lake Constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances. Applied and Environmental Microbiology 74, 7740–7749.
| Bacteria associated with benthic diatoms from Lake Constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnvVai&md5=178ea581036ef57813fc43a87c50e8f7CAS | 18931294PubMed |
Bruckner, C. G., Grossart, H.-P., Rehm, C., and Kroth, P. G. (2011). Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria. Environmental Microbiology 13, 1052–1063.
| Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtV2jtr4%3D&md5=77e93375240fa713e82fb64e38474b15CAS | 21244599PubMed |
Buchanan, J. B. (1984). Methods for the study of marine benthos. In ‘Macrofauna Techniques’. (Eds N.A. Holme and A. D. McIntyre.) pp. 41–65. (Blackwell Scientific Publications: London.)
Buric, Z., Caput, K., and Vilicic, D. (2004). Distribution of the diatom Cocconeis scutellum in the karstic estuary (Zrmanja, eastern Adriatic Sea). Biologia 59, 1–7.
Cattaneo, A. (1990). The effect of fetch on periphyton spatial variation. Hydrobiologia 206, 1–10.
| The effect of fetch on periphyton spatial variation.Crossref | GoogleScholarGoogle Scholar |
Cavanaugh, G. M. (1975). ‘Formulae and Methods of the Marine Biological Chemical Room’, 6th edn. (Marine Biological Laboratory: Woods Hole.)
Clarke, K. R., and Gorley, R. N. (2006). ‘PRIMER v.6: User Manual/Tutorial.’ (PRIMER-E: Plymouth, UK.)
Clarke, K. R., and Warwick, R. M. (2001). ‘Change in Marine Communities: An Approach to Statistical Analyses and Interpretation.’ (Plymouth Marine Laboratory: Plymouth, UK)
Dale, N. G. (1974). Bacteria in intertidal sediments: factors related to their distribution. Limnology and Oceanography 19, 509–518.
| Bacteria in intertidal sediments: factors related to their distribution.Crossref | GoogleScholarGoogle Scholar |
D’Costa, P. M., and Anil, A. C. (2010). Diatom community dynamics in a tropical, monsoon-influenced environment: west coast of India. Continental Shelf Research 30, 1324–1337.
| Diatom community dynamics in a tropical, monsoon-influenced environment: west coast of India.Crossref | GoogleScholarGoogle Scholar |
D’Costa, P. M., and Anil, A. C. (2011). The effect of bacteria on diatom community structure: the ‘antibiotics’ approach. Research in Microbiology 162, 292–301.
| The effect of bacteria on diatom community structure: the ‘antibiotics’ approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVOktLY%3D&md5=4d1b1e2a027e1c91dabba20225a54945CAS | 21194562PubMed |
D’Costa, P. M., Anil, A. C., Patil, J. S., Hegde, S., D’Silva, M. S., and Chourasia, M. (2008). Dinoflagellates in a mesotrophic, tropical environment influenced by monsoon. Estuarine, Coastal and Shelf Science 77, 77–90.
| Dinoflagellates in a mesotrophic, tropical environment influenced by monsoon.Crossref | GoogleScholarGoogle Scholar |
Desbois, A. P., Walton, M., and Smith, V. J. (2010). Differential antibacterial activities of fusiform and oval morphotypes of Phaeodactylum tricornutum (Bacillariophyceae). Journal of the Marine Biological Association of the United Kingdom 90, 769–774.
| Differential antibacterial activities of fusiform and oval morphotypes of Phaeodactylum tricornutum (Bacillariophyceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1CnsL4%3D&md5=e61311e8530d3020e88fba93089191f1CAS |
Desikachary, T. V., and Prema, P. (1987). Diatoms from the Bay of Bengal. In ‘Atlas of Diatoms. Fascicles III and IV.’ (Ed. T. V. Desikachary.) pp. 222–331. (TT Maps and Publications: Madras.)
Desikachary, T. V., Gowthaman, S., and Latha, Y. (1987a). Diatom flora of some sediments from the Indian Ocean region. In ‘Atlas of Diatoms. Fascicle II.’ (Ed. T. V. Desikachary.) pp. 78–221. (TT Maps and Publications: Madras.)
Desikachary, T. V., Hema, A., Prasad, A. K. S. K., Sreelatha, P. M., Sridharan, V. T., and Subrahmanyan, R. (1987b). Marine diatoms from the Arabian Sea and Indian Ocean. In ‘Atlas of Diatoms. Fascicle IV.’ (Ed. T. V. Desikachary.) pp. 332–400A. (TT Maps and Publications: Madras.)
Fukami, K., Nishijima, T., and Ishida, Y. (1997). Stimulatory and inhibitory effects of bacteria on the growth of microalgae. Hydrobiologia 358, 185–191.
| Stimulatory and inhibitory effects of bacteria on the growth of microalgae.Crossref | GoogleScholarGoogle Scholar |
Gerbersdorf, S. U., Bittner, R., Lubarsky, H., Manz, W., and Paterson, D. M. (2009). Microbial assemblages as ecosystem engineers of sediment stability. Journal of Soils and Sediments 9, 640–652.
| Microbial assemblages as ecosystem engineers of sediment stability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlyns73N&md5=de4c88d56431153469afcc4782c872bfCAS |
Goto, N., Kawamura, T., Mitamura, O., and Terai, H. (1999). Importance of extracellular organic carbon production in the total primary production by tidal-flat diatoms in comparison to phytoplankton. Marine Ecology Progress Series 190, 289–295.
| Importance of extracellular organic carbon production in the total primary production by tidal-flat diatoms in comparison to phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtl2jtLY%3D&md5=5e545837ff1a12f25e4ec77e426431c9CAS |
Guillard, R. R. L., and Ryther, J. H. (1962). Studies of marine planktonic diatoms. I. Cyclotella nana Husted and Detonula confervacea (Cleve) Gran. Canadian Journal of Microbiology 8, 229–239.
| Studies of marine planktonic diatoms. I. Cyclotella nana Husted and Detonula confervacea (Cleve) Gran.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XktlWqu70%3D&md5=58f68fd63b2467fcf58081f236796ed1CAS |
Harris, A. S. D., Jones, K. J., and Lewis, J. (1998). An assessment of the accuracy and reproducibility of the most probable number (MPN) technique in estimating numbers of nutrient stressed diatoms in sediment samples. Journal of Experimental Marine Biology and Ecology 231, 21–30.
| An assessment of the accuracy and reproducibility of the most probable number (MPN) technique in estimating numbers of nutrient stressed diatoms in sediment samples.Crossref | GoogleScholarGoogle Scholar |
Haynes, K., Hofman, T. A., Smith, C. J., Ball, A. S., Underwood, G. J. C., and Osborn, A. M. (2007). Diatom-derived carbohydrates as factors affecting bacterial community composition in estuarine sediments. Applied and Environmental Microbiology 73, 6112–6124.
| Diatom-derived carbohydrates as factors affecting bacterial community composition in estuarine sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGmtrrJ&md5=c671866fd9052cb277b2feff433a89beCAS | 17675437PubMed |
Hillebrand, H., and Cardinale, B. J. (2004). Consumer effects decline with prey diversity. Ecology Letters 7, 192–201.
| Consumer effects decline with prey diversity.Crossref | GoogleScholarGoogle Scholar |
Holt, J. G., Krieg, N. R., Sneath, P. H. A., Staley, J. T., and Williams, S. T. (1994). ‘Bergey’s Manual of Determinative Bacteriology’, 9th edn. (Williams and Wilkins: Baltimore.)
Horner, R. A. (2002). ‘A Taxonomic Guide to Some Common Marine Phytoplankton.’ (Biopress: Bristol.)
Hulot, F. D., and Huisman, J. (2004). Allelopathic interactions between phytoplankton species: The roles of heterotrophic bacteria and mixing intensity. Limnology and Oceanography 49, 1424–1434.
| Allelopathic interactions between phytoplankton species: The roles of heterotrophic bacteria and mixing intensity.Crossref | GoogleScholarGoogle Scholar |
Imai, I., and Itakura, S. (1999). Importance of cysts in the population dynamics of the red tide flagellate Heterosigma akashiwo (Raphidophyceae). Marine Biology 133, 755–762.
| Importance of cysts in the population dynamics of the red tide flagellate Heterosigma akashiwo (Raphidophyceae).Crossref | GoogleScholarGoogle Scholar |
Jordan, L., McMinn, A., and Wotherspoon, S. (2008). Diurnal and monthly vertical profiles of benthic microalgae within intertidal sediments from two temperate localities. Marine and Freshwater Research 59, 931–939.
| Diurnal and monthly vertical profiles of benthic microalgae within intertidal sediments from two temperate localities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1yqsrbE&md5=92627e01f251b161c3c1f65068ca3534CAS |
Koh, C. H., Khim, J. S., Araki, H., Yamanishi, H., and Koga, K. (2007). Within-day and seasonal patterns of microphytobenthos biomass determined by co-measurement of sediment and water column chlorophylls in the intertidal mudflat of Nanaura, Saga, Ariake Sea, Japan. Estuarine, Coastal and Shelf Science 72, 42–52.
| Within-day and seasonal patterns of microphytobenthos biomass determined by co-measurement of sediment and water column chlorophylls in the intertidal mudflat of Nanaura, Saga, Ariake Sea, Japan.Crossref | GoogleScholarGoogle Scholar |
Kovach, W. (1998). ‘Multi-variate Statistical package. Ver.3.01.’ (Kovach Computing Services: Pentraeth, Wales, UK.)
Kuipers, B. R., De Wilde, P. A. W. J., and Crentzberg, F. (1981). Energy flow in a tidal flat ecosystem. Marine Ecology Progress Series 5, 215–221.
| Energy flow in a tidal flat ecosystem.Crossref | GoogleScholarGoogle Scholar |
Levkov, Z. (2009). Amphora sensu lato. In ‘Diatoms of Europe: Diatoms of the European Inland Waters and Comparable Habitats. Vol. 5.’ (Ed. H. Lange-Bertalot.) pp. 5–916. (A. R. G. Gantner Verlag: Ruggell.)
Long, R. A., Rowley, D. C., Zamora, E., Liu, J., Bartlett, D. H., and Azam, F. (2005). Antagonistic interactions among marine bacteria impede the proliferation of Vibrio cholerae. Applied and Environmental Microbiology 71, 8531–8536.
| Antagonistic interactions among marine bacteria impede the proliferation of Vibrio cholerae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlehtbrL&md5=1651538d543da8bb61bddd7437a838cbCAS | 16332844PubMed |
Lubarsky, H. V., Hubas, C., Chocholek, M., Larson, F., Manz, W., Paterson, D. M., and Gerbersdorf, S. U. (2010). The stabilisation potential of individual and mixed assemblages of natural bacteria and microalgae. PLoS One 5, e13794.
| The stabilisation potential of individual and mixed assemblages of natural bacteria and microalgae.Crossref | GoogleScholarGoogle Scholar | 21072186PubMed |
MacIntyre, H. L., Geider, R. J., and Miller, D. C. (1996). Microphytobenthos: the ecological role of the ‘secret garden’ of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19, 186–201.
| Microphytobenthos: the ecological role of the ‘secret garden’ of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production.Crossref | GoogleScholarGoogle Scholar |
Makk, J., Acs, E., Marialigeti, K., and Kovacs, G. (2003). Investigations on the Danube gravel–biofilm diatom-associated bacterial communities. Biologia 58, 729–742.
Maruyama, A., Maeda, M., and Simidu, U. (1986). Occurrence of plant hormone (cytokinin)-producing bacteria in the sea. The Journal of Applied Bacteriology 61, 569–574.
| Occurrence of plant hormone (cytokinin)-producing bacteria in the sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhtFKhsLk%3D&md5=d1530400daf0f997b3b15845d5568587CAS |
McMinn, A., Sellah, S., Llah, W. A. W. A., Mohammad, M., Merican, F. M. S., Omar, W. M. W., Samad, F., Cheah, W., Idris, I., Sim, Y. K., Wong, W. S., Tan, S. H., and Yasin, Z. (2005). Quantum yield of the marine benthic microflora of near-shore coastal Penang, Malaysia. Marine and Freshwater Research 56, 1047–1053.
| Quantum yield of the marine benthic microflora of near-shore coastal Penang, Malaysia.Crossref | GoogleScholarGoogle Scholar |
Middelburg, J. J., Barranguet, C., Boschker, H. T. S., Herman, P. M. J., Moens, T., and Heip, C. H. R. (2000). The fate of intertidal microphytobenthos carbon: An in situ 13C-labeling study. Limnology and Oceanography 45, 1224–1234.
| The fate of intertidal microphytobenthos carbon: An in situ 13C-labeling study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFCitLo%3D&md5=eda60359a2785c4ff25699f90fde73caCAS |
Mitbavkar, S., and Anil, A. C. (2002). Diatoms of the microphytobenthic community: population structure in a tropical, intertidal sand flat. Marine Biology 140, 41–57.
| Diatoms of the microphytobenthic community: population structure in a tropical, intertidal sand flat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisVGrs7c%3D&md5=c638fa3b0ee8d38fecd8bddf82892071CAS |
Mitbavkar, S., and Anil, A. C. (2004). Vertical migratory rhythms of benthic diatoms in a tropical intertidal sand flat: influence of irradiance and tides. Marine Biology 145, 9–20.
| Vertical migratory rhythms of benthic diatoms in a tropical intertidal sand flat: influence of irradiance and tides.Crossref | GoogleScholarGoogle Scholar |
Mitbavkar, S., and Anil, A. C. (2006). Diatoms of the microphytobenthic community in a tropical intertidal sand flat influenced by monsoons: spatial and temporal variations. Marine Biology 148, 693–709.
| Diatoms of the microphytobenthic community in a tropical intertidal sand flat influenced by monsoons: spatial and temporal variations.Crossref | GoogleScholarGoogle Scholar |
Parsons, T. R., Maita, Y., and Lalli, C. M. (1984). ‘Manual of Chemical and Biological Methods for Seawater Analysis.’ (Pergamon Press: New York.)
Round, F. E. (1965). The epipsammon: a relatively unknown freshwater algal association. British Phycological Bulletin 2, 456–462.
| The epipsammon: a relatively unknown freshwater algal association.Crossref | GoogleScholarGoogle Scholar |
Round, F. E. (1979). Occurrence and rhythmic behaviour of Tropidoneis lepidoptera in the epipelon of Barnstable Harbor, Massachusetts, USA. Marine Biology 54, 215–217.
| Occurrence and rhythmic behaviour of Tropidoneis lepidoptera in the epipelon of Barnstable Harbor, Massachusetts, USA.Crossref | GoogleScholarGoogle Scholar |
Sabbe, K. (1993). Short-term fluctuations in benthic diatom numbers on an intertidal sandflat in the Westerschelde estuary (Zeeland, The Netherlands). Hydrobiologia 269–270, 275–284.
| Short-term fluctuations in benthic diatom numbers on an intertidal sandflat in the Westerschelde estuary (Zeeland, The Netherlands).Crossref | GoogleScholarGoogle Scholar |
Schäfer, H., Abbas, B., Witte, H., and Muyzer, G. (2002). Genetic diversity of ‘satellite’ bacteria present in cultures of marine diatoms. FEMS Microbiology Ecology 42, 25–35.
| 19709263PubMed |
Scheffer, M., van Nes, E. H., Holmgren, M., and Hughes, T. (2008). Pulse-driven loss of top-down control: the critical-rate hypothesis. Ecosystems 11, 226–237.
| Pulse-driven loss of top-down control: the critical-rate hypothesis.Crossref | GoogleScholarGoogle Scholar |
Scholz, B., and Liebezeit, G. (2012). Microphytobenthic dynamics in a Wadden Sea intertidal flat: part I: Seasonal and spatial variation of diatom communities in relation to macronutrient supply. European Journal of Phycology 47, 105–119.
| Microphytobenthic dynamics in a Wadden Sea intertidal flat: part I: Seasonal and spatial variation of diatom communities in relation to macronutrient supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotFaju70%3D&md5=6b22cc1ed09b2b85973ae47405bac0a0CAS |
Semenitz, E. (1983). Mechanism of action of beta-lactam antibiotics and problems concerning the development of resistance in antibacterial chemotherapy. Wiener Klinische Wochenschrift Supplementum 142, 7–11.
| 1:STN:280:DyaL2c%2FnsFemtA%3D%3D&md5=83a41b5ad1fa9a351ce779b427adc650CAS | 6606272PubMed |
Smith, D. J., and Underwood, G. J. C. (1998). Exopolymer production by intertidal epipelic diatoms. Limnology and Oceanography 43, 1578–1591.
| Exopolymer production by intertidal epipelic diatoms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvV2q&md5=b147e8a275c5b5c8c54dd506ea0a0444CAS |
Strickland, J. D. H., and Parsons, T. R. (1965). ‘A Manual of Seawater Analysis’, 2nd edn. (Queen’s Printer and Controller of Stationery: Ottawa.)
Subrahmanyan, R. (1946). A systematic account of the marine phytoplankton diatoms of the Madras coast. Proceedings of the Indian Academy of Sciences 24, 85–197.
Sundbäck, K., Miles, A., and Goransson, E. (2000). Nitrogen fluxes, denitrification and the role of microphytobenthos in micro-tidal shallow-water sediments: an annual study. Marine Ecology Progress Series 200, 59–76.
| Nitrogen fluxes, denitrification and the role of microphytobenthos in micro-tidal shallow-water sediments: an annual study.Crossref | GoogleScholarGoogle Scholar |
ter Braak, C. J. F. (1995). Ordination. In ‘Data Analysis in Community and Landscape Ecology’. (Eds R. H. G. Jongman, C. J. F. ter Braak, O. F. R. van Tongeren.) pp. 91–173. (Cambridge University Press, Cambridge.)
Throndsen, J. (1978). The dilution-culture method. In ‘UNESCO Monographs on Oceanographic Methodology, Vol. 6, Phytoplankton Manual.’ (Ed. A. Sournia.) pp. 218–224. (UNESCO Publishing: Paris.)
Tomas, C. R. (ed) (1997). ‘Identifying Marine Phytoplankton.’ (Academic Press: San Diego, CA.)
Wigglesworth-Cooksey, B., Berglund, D., and Cooksey, K. E. (2001). Cell–cell and cell–surface interactions in an illuminated biofilm: implications for marine sediment stabilization. Geochemical Transactions 2, 75–82.
| Cell–cell and cell–surface interactions in an illuminated biofilm: implications for marine sediment stabilization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zks1Kltg%3D%3D&md5=c60c2bce896d6b1951dbae8ebf67d777CAS | 16759422PubMed |
Witkowski, A., Lange-Bertalot, H., and Metzeltin, D. (2000). Diatom flora of marine coasts, I. In ‘Iconographia Diatomologica. Annotated Diatom Micrographs. Diversity–Taxonomy–Identification. Vol. 7.’ (Ed. H. Lange-Bertalot.), pp. 1–925. (A. R. G. Gantner Verlag: Ruggell.)