Tidal Stage Changes in Structure and Diversity of Intertidal Benthic Diatom Assemblages: a Case Study from Two Contrasting Charleston Harbor Flats
Benthic microalgae are key contributors to near-shore food webs and sediment stabilization. Temporal variability in microalgal biomass and production throughout the tidal cycle has been well documented; however, due to limitations of traditional methods of analysis patterns of community composition and diversity over such time scales have not been revealed. To explore the latter and better understand how short-term changes throughout the tidal cycle may affect community functioning, we compared benthic diatom composition and diversity over tidal stage shifts. We employed two disparate molecular techniques (denaturing gel gradient electrophoresis with Sanger DNA sequencing of excised bands and high-throughput community metagenome sequencing) to characterize diatom assemblages in representative muddy and sandy intertidal sites in Charleston Harbor, SC, USA. In support of prior studies, we found higher diatom diversity in sandbar as compared to mudflat sediments. Spatial differences were stronger relative to tidal temporal differences, although diversity metrics generally were highest after prolonged tidal immersion as compared to low-tide emersion or just after immersion at flood tide. Composition of the diatom assemblage differed markedly between sites, with species in genera Halamphora, Amphora, and Navicula dominating the sandbar, whereas Cyclotella, Skeletonema, and Thalassiosira were the most prevalent genera on the mudflat. Diatom composition differed by tidal stage, with assemblages during low-tide exposure distinct from samples taken after immersion. Both sandbar and mudflat sediments exhibited increases in relative proportion of epipelic diatoms and decreases in planktonic taxa during low-tide exposure. Our findings of short-term changes in species composition and dominance could inform primary productivity models to better estimate understudied diatom contributions in heterogeneous and highly variable tidal systems.
KeywordsBenthic microalgae Diatom Sediment Resuspension South Carolina High-throughput sequencing
We thank the directors of the Fort Johnson Summer REU Program, Drs. Louis and Karen Burnett. Also, we thank Patricia Roth for her experimental thoroughness and advice. This report is based upon work supported by the US National Science Foundation under grant DBI-1062990. This is contribution no. 494 of the Grice Marine Laboratory.
- Aguilera, A., F. Gómez, E. Lospitao, and R. Amils. 2006. A molecular approach to the characterization of the eukaryotic communities of an extreme acidic environment: methods for DNA extraction and denaturing gradient gel electrophoresis analysis. Systematic and Applied Microbiology 29: 593–605.CrossRefGoogle Scholar
- Brockmann, C. 1950. Die Watt-Diatomeen de schleswig-holsteinischen Westküste. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 487: 1–26.Google Scholar
- Caporaso, J.G., J. Kuczynski, J. Stombaugh, K. Bittinger, F.D. Bushman, E.K. Costello, N. Fierer, A.G. Pena, J.K. Goodrich, J.I. Gordon, G.A. Huttley, S.T. Kelley, D. Knights, J.E. Koenig, R.E. Ley, C.A. Lozupone, D. McDonald, B.D. Muegge, M. Pirrung, J. Reeder, J.R. Sevinsky, P.J. Turnbaugh, W.A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, and R. Knight. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335–336.CrossRefGoogle Scholar
- Cary, S.C., B.J. Hicks, N.J. Crawford, and K.A. Coyne. 2006. A sensitive genetic-based detection capability for Didymosphenia geminate. Interim report: CBER contract report. Vol. 45, 68 pp. Hamilton: Centre for Biodiversity and Ecology Research.Google Scholar
- Clarke, K.R., and R.N. Gorley. 2006. Primer v6: user manual/tutorial. Plymouth: PRIMER-E.Google Scholar
- de Jonge, V.N. 1994. Wind-driven tidal and annual gross transport of mud and microphytobenthos in the Ems estuary, and its importance for the ecosystem. In Changes in fluxes in estuaries, ed. K.R. Dyer and R.J. Orth, 29–40. Fredensborg: Olsen and Olsen.Google Scholar
- Diez, B., C. Pedros-Alio, T.L. Marsh, and R. Massana. 2001. Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Applied and Environmental Microbiology 67: 2942–2951.CrossRefGoogle Scholar
- Graf, G. 1992. Benthic-pelagic coupling: a benthic view. Oceanography and Marine Biology: An Annual Review 30: 149–190.Google Scholar
- Guillard, R.R.L. 1975. Culture of phytoplankton for feeding marine invertebrates. In Culture of marine invertebrate animals, ed. W.L. Smith and M.H. Chanley, 26–60. Plenum: New York.Google Scholar
- Hamady, M., C. Lozupone, and R. Knight. 2009. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. Int Society Microbial Ecology J 4: 17–27.Google Scholar
- Hamels, I., K. Sabbe, K. Muylaert, C. Barranguet, C. Lucas, P. Herman, and W. Vyverman. 1998. Organisation of microbenthic communities in intertidal estuarine flats, a case study from the Molenplaat (Westerschelde estuary, the Netherlands). European Journal of Protistology 34: 308–320.CrossRefGoogle Scholar
- Hustedt, F. 1939. Die Diatomeenflora des Kustengebietes der Nordsee vom Dollart bis zur Elbmündung. I. Die Diatomeenflora in den Sedimenten der unteren Ems sowie auf den Watten der Leybucht, des Memmert und bei der Insel Juist. Adhandlungen des Naturwissenschaftlichen Verein zu Bremen 31: 571–677.Google Scholar
- Madden, T. 2002. The BLAST sequence analysis tool. In The NCBI handbook, ed. J. McEntyre and J. Ostell CH, 16. Bethesda (MD): National Center for Biotechnology Information (US) Available from: http://www.ncbi.nlm.nih.gov/books/NBK21097/ .
- Muyzer, G., E.C. de Waal, and A.G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied Environmental Microbiology 59: 695–700.Google Scholar
- Rees, G.N., D.S. Baldwin, G.O. Watson, S. Perryman, and D.L. Nielsen. 2004. Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie Van Leeuwenhoek 86: 339–347.CrossRefGoogle Scholar
- Riaux, C. 1982. La chlorophylle a dans un sédiment estuarien de Bretagne Nord. Annales de l’Institut Océanographique 58: 185–203.Google Scholar
- Ribeiro, L.L.C.S. 2010. Intertidal benthic diatoms of the Tagus estuary: taxonomic composition and spatial-temporal variation. Ph.D. dissertation. Lisbon: Universidade de Lisboa.Google Scholar
- Sabbe, K. 1997. Systematics and ecology of intertidal benthic diatoms of the Westerschelde Estuary (the Netherlands). Ph.D. dissertation. Ghent: Universiteit Gent.Google Scholar
- Sabbe, K., and W. Vyverman. 1991. Distribution of benthic diatom assemblages in the Westerschelde (Zeeland, the Netherlands). Belgium Journal Botany 124: 91–101.Google Scholar
- Underwood, G.J.C., R.G. Perkins, M.C. Consalvey, A.R.M. Hanlon, K. Oxborough, N.R. Baker, and D.M. Paterson. 2005. Patterns in microphytobenthic primary productivity: species-specific variation in migratory rhythms and photosynthetic efficiency in mixed-species biofilms. Limnology and Oceanography 50: 755–767.CrossRefGoogle Scholar