Browse > Article
http://dx.doi.org/10.4490/algae.2018.33.4.3

Next-generation sequencing reveals the diversity of benthic diatoms in tidal flats  

An, Sung Min (Marine Ecosystem and Biological Research Center, Korea Institute of Ocean Science & Technology)
Choi, Dong Han (Marine Ecosystem and Biological Research Center, Korea Institute of Ocean Science & Technology)
Lee, Howon (Marine Ecosystem and Biological Research Center, Korea Institute of Ocean Science & Technology)
Lee, Jung Ho (Department of Biology Education, Daegu University)
Noh, Jae Hoon (Marine Ecosystem and Biological Research Center, Korea Institute of Ocean Science & Technology)
Publication Information
ALGAE / v.33, no.2, 2018 , pp. 167-180 More about this Journal
Abstract
Benthic diatoms are ubiquitous in tidal flats and play major roles in maintaining coastal ecosystems. Spatio-temporal variations in diatom diversity have not been well-studied, mainly because of difficulties in morphological identification and the lack of appropriate genetic tools. To overcome these problems, we used the gene encoding the ribulose bisphosphate carboxylase large-subunit (rbcL) as a molecular marker, and sequenced these genes with the aid of the MiSeq platform. In this manner, we explored the genetic diversity of benthic diatoms in tidal flats of Guenso Bay on the west coast of Korea; differences in the spatial distributions of benthic diatoms were evident. The diatom communities were dominated by Nitzschia, Navicula, and Amphora; their relative distributions were affected by the sand proportion, grain size, and air exposure time. Our results suggest that meta-barcoding of the rbcL gene and next-generation sequencing can be used to explore the diversity of benthic diatoms.
Keywords
benthic diatom; diversity; MiSeq; rbcL gene; tidal flat;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Mitbavkar, S. & Anil, A. 2002. Diatoms of the microphytobenthic community: population structure in a tropical intertidal sand flat. Mar. Biol. 140:41-57.   DOI
2 Moniz, M. B. J. & Kaczmarska, I. 2010. Barcoding of diatoms: nuclear encoded ITS revisited. Protist 161:7-34.   DOI
3 Nanjappa, D., Audic, S., Romac, S., Kooistra, W. H. & Zingone, A. 2014. Assessment of species diversity and distribution of an ancient diatom lineage using a DNA metabarcoding approach. PLoS ONE 9:e103810.   DOI
4 Oh, S. J., Yoon, Y. H., Yamamoto, T. & Yang, H. -S. 2009. Effect of attachment substrate size on the growth of a benthic microalgae Nitzschia sp. in culture condition. J. Korean Soc. Mar. Environ. Energy 12:91-95.
5 Park, S. K., Kim, B. Y., Choi, H. G., Oh, J. -S., Chung, S. -O., An, K. -H. & Park, K. -J. 2013. Seasonal variation in species composition and biomass of microphytobenthos at Jinsanri, Taean, Korea. Korean J. Fish. Aquat. Sci. 46:176-185.
6 Parsons, T. R., Maita, Y. & Lalli, C. M. 1984. A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, 173 pp.
7 Rejil, T. 2013. Microalgal vegetation in the selected Mangrove Ecosystems of Kerala. Ph.D. dissertation, Cochin University of Science and Technology, Kalamassery, 262 pp.
8 Roer, R. D. 2008. A genetic marker for coastal diatoms based on psbA. M.S. thesis, University of North Carolina, Wilmington, NC, 64 pp.
9 Round, F. E. 1971. Benthic marine diatoms. Oceanogr. Mar. Biol. Ann. Rev. 9:83-139.
10 Admiraal, W. 1976. Influence of light and temperature on the growth rate of estuarine benthic diatoms in culture. Mar. Biol. 39:1-9.
11 Admiraal, W. 1984. The ecology of estuarine sediment-inhabiting diatoms. Prog. Phycol. Res. 3:269-322.
12 Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313.   DOI
13 Sato, S., Kooistra, W. H. C. F., Watanabe, T., Matsumoto, S. & Medlin, L. K. 2008. A new araphid diatom genus Psammoneis gen. nov. (Plagiogrammaceae, Bacillariophyta) with three new species based on SSU and LSU rDNA sequence data and morphology. Phycologia 47:510-528.   DOI
14 Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J. & Weber, C. F. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microb. 75:7537-7541.   DOI
15 Shokralla, A., Spall, J. L., Gibson, J. F. & Hajibabaei, M. 2012. Next-generation sequencing technologies for environmental DNA research. Mol. Ecol. 21:1794-1805.   DOI
16 Stief, P., Kamp, A. & de Beer, D. 2013. Role of diatoms in the spatial-temporal distribution of intracellular nitrate in intertidal sediment. PLoS ONE 8:e73257.   DOI
17 Sullivan, M. J. & Moncreiff, C. A. 1988. Primary production of euphotic algal communities in a Mississippi salt marsh. J. Phycol. 24:49-58.
18 Ter Braak, C. J. & Smilauer, P. 2002. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Available from: http://www.canoco5.com/. Accessed Sep 20, 2017.
19 Theriot, E. C., Cannone, J. J., Gutell, R. R. & Alverson, A. J. 2009. The limits of nuclear-encoded SSU rDNA for resolving the diatom phylogeny. Eur. J. Phycol. 44:277-290.   DOI
20 Trobajo, R., Mann, D. G., Clavero, E., Evans, K. M., Vanormelingen, P. & McGregor, R. C. 2010. The use of partial cox1, rbcL and LSU rDNA sequences for phylogenetics and species identification within the Nitzschia palea species complex (Bacillariophyceae). Eur. J. Phycol. 45:413-425.   DOI
21 Underwood, G. J. C. 1994. Seasonal and spatial variation in epipelic diatom assemblages in the Severn estuary. Diatom Res. 9:451-472.   DOI
22 Underwood, G. J. C. & Barnett, M. 2006. What determines species composition inmicrophytobenthic biofilms? In Kromkamp, J. C., de Brouwer, J. F. C., Blanchard, G. F., Forster, R. M. & Creach, V. (Eds.) Functioning of Microphytobenthos in Estuaries. Royal Netherlands Academy of Arts and Sciences, Amsterdam, pp. 121-138.
23 Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M. & Rozen, S. G. 2012. Primer3: new capabilities and interfaces. Nucleic Acids Res. 40:e115.   DOI
24 Visco, J. A., Apotheloz-Perret-Gentil, L., Cordonier, A., Esling, P., Pillet, L. & Pawlowski, J. 2015. Environmental monitoring: inferring the diatom index from next-generation sequencing data. Environ. Sci. Technol. 49:7597-7605.   DOI
25 Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.   DOI
26 Watermann, F., Hillebrand, H., Gerdes, G., Krumbein, W. E. & Sommer, U. 1999. Competition between benthic cyanobacteria and diatoms as influenced by different grain sizes and temperatures. Mar. Ecol. Prog. Ser. 187:77-87.   DOI
27 Zimmermann, J., Glockner, G., Jahn, R., Enke, N. & Gemeinholzer, B. 2015. Metabarcoding vs. morphological identification to assess diatom diversity in environmental studies. Mol. Ecol. Resour. 15:526-542.   DOI
28 Yallop, M. L., de Winder, B., Paterson, D. M. & Stal, L. J. 1994. Comparative structure, primary production and bio-genic stabilization of cohesive and non-cohesive marine sediments inhabited by microphytobenthos. Estuar. Coast. Shelf Sci. 39:565-582.   DOI
29 Yarza, P., Yilmaz, P., Pruesse, E., Glockner, F. O., Ludwig, W., Schleifer, K. -H., Whitman, W. B., Euzeby, J., Amann, R. & Rossello-Mora, R. 2014. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat. Rev. Microbiol. 12:635-645.   DOI
30 Yoo, M. H. 2004. Seasonal distribution of microphytobenthos and primary production on an intertidal mud flat in Janghwa, Ganghwa Island of Korea. M.S. thesis, Inha University, Incheon, 96 pp.
31 Zimmermann, J., Jahn, R. & Gemeinholzer, B. 2011. Barcoding diatoms: evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols. Org. Divers. Evol. 11:173-192.   DOI
32 Beszteri, B., Acs, E., Makk, J., Kovacs, G., Marialigeti, K. & Kiss, K. T. 2001. Phylogeny of six naviculoid diatoms based on 18S rDNA sequences. Int. J. Syst. Evol. Microbiol. 51:1581-1586.   DOI
33 Amato, A., Kooistra, W. H. C. F., Ghiron, J. H. L., Mann, D. G., Proschold, T. & Montresor, M. 2007. Reproductive isolation among sympatric cryptic species in marine diatoms. Protist 158:193-207.   DOI
34 An, S. M., Choi, D. H., Lee, J. H., Lee, H. & Noh, J. H. 2017. Identification of benthic diatoms isolated from the eastern tidal flats of the Yellow Sea: comparison between morphological and molecular approaches. PLoS ONE 12:e0179422.   DOI
35 Baldi, F., Facca, C., Marchetto, D., Nguyen, T. N. M. & Spurio, R. 2011. Diatom quantification and their distribution with salinity brines in coastal sediments of Terra Nova Bay (Antarctica). Mar. Environ. Res. 71:304-311.   DOI
36 Blott, S. J. & Pye, K. 2001. GRADISTAT: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surf. Proc. Land. 26:1237-1248.   DOI
37 Choi, H. C. 2002. A study on the microphytobenthos on an intertidal mud flat of Ganghwa is. in Korea. M.S. thesis, Inha University, Incheon, Korea, 67 pp.
38 Bruder, K. & Medlin, L. K. 2008. Morphological and molecular investigations of naviculoid diatoms. II. Selected genera and families. Diatom Res. 23:283-329.   DOI
39 Carver, T. & Bleasby, A. 2003. The design of Jemboss: a graphical user interface to EMBOSS. Bioinformatics 19:1837-1843.   DOI
40 Choi, D. H., Noh, J. H., An, S. M., Choi, Y. R., Lee, H., Ra, K., Kim, D., Rho, T., Lee, S. H., Kim, K. -T., Chang, K. -I. & Lee, J. H. 2016. Spatial distribution of cold-adapted Synechococcus during spring in seas adjacent to Korea. Algae 31:231-241.   DOI
41 De Seve, M. A., Poulin, P., Pelletier, E. & Lemarchand, K. 2010. Benthic diatom communities from two salt marshes of the St. Lawrence estuary (Canada). J. Water Sci. 23:349-358.
42 Choi, J. -K., Ryu, J. -H., Woo, H. J. & Eom, J. 2011. A study on the flushing characteristics in Geunso bay using hydrohypsographic analysis. J. Wetlands Res. 13:45-52.
43 Cibic, T., Blasutto, O., Hancke, K., & Johnsen, G. 2007. Microphytobenthic species composition, pigment concentration, and primary production in sublittoral sediments of the Trondheimsfjord (Norway). J. Phycol. 43:1126-1137.   DOI
44 Delaney, J. A., Ulrich, R. M. & Paul, J. H. 2011. Detection of the toxic marine diatom Pseudo-nitzschia multiseries using the RuBisCO small subunit (rbcS) gene in two real-time RNA amplification formats. Harmful Algae 11:54-64.   DOI
45 Hajibabaei, M., Spall, J. L., Shokralla, S. & Van Konynenburg, S. 2012. Assessing biodiversity of a freshwater benthic macroinvertebrate community through non-destructive environmental barcoding of DNA from preservative ethanol. BMC Ecol. 12:28.   DOI
46 Dijkema, K. S. & Wolff, W. J. 1983. Flora and vegetation of the Wadden Sea islands and coastal areas. August Aime Balkema, Rotterdam, 413 pp.
47 Ehara, M., Inagaki, Y., Watanabe, K. I. & Ohama, T. 2000. Phylogenetic analysis of diatom cox1 genes and implications of a fluctuating GC content on mitochondrial genetic code evolution. Curr. Genet. 37:29-33.   DOI
48 Evans, K. M., Wortley, A. H. & Mann, D. G. 2007. An assessment of potential diatom "Barcode" genes (cox1, rbcL, 18S and ITS rDNA) and their effectiveness in determining relationships in Sellaphora (Bacillariophyta). Protist 158:349-364.   DOI
49 Hamsher, S. E., Evans, K. M., Mann, D. G., Poulickova, A. & Saunders, G. W. 2011. Barcoding diatoms: exploring alternatives to COI-5P. Protist 162:405-422.   DOI
50 Hamels, I., Sabbe, K., Muyleart, K., Barranguet, C., Lucas, C., Herman, P. & Vyverman, W. 1998. Organisation of microbenthic communities in intertidal estuarine flats, a case study from the Molenplaat (Westerschelde estuary, The Netherlands). Eur. J. Protistol. 34:308-320.   DOI
51 Haubois, A. -G., Sylvestre, F., Guarini, J. -M., Richard, P. & Blanchard, G. F. 2005. Spatio-temporal structure of the epipelic diatom assemblage from an intertidal mudflat in Marennes-Oleeron Bay, France. Estuar. Coast. Shelf Sci. 64:385-394.   DOI
52 Jones, H. M., Simpson, G. E., Stickle, A. J. & Mann, D. G. 2005. Life history and systematics of Petroneis (Bacillariophyta), with special reference to British waters. Eur. J. Phycol. 40:61-87.   DOI
53 Hughes, E. H. & Sherr, E. B. 1983. Subtidal food webs in a Georgia estuary: ${\delta}^{13}$ C analysis. J. Exp. Mar. Biol. Ecol. 67:227-242.   DOI
54 Illumina. 2013. 16S metagenomic sequencing library preparation. Available from: http://support.illumina.com/downloads/16s_metagenomic_sequencing_library_preparation.html. Accessed Sep 20, 2017.
55 Jiang, S., Pang, G., Wu, M. & Kuang, L. 2012. An improved K nearest-neighbor algorithm for text categorization. Expert Syst. Appl. 39:1503-1509.   DOI
56 Kermarrec, L., Franc, A., Rimet, F., Chaumeil, P., Frigerio, J. -M., Humbert, J. -F. & Bouchez, A. 2014. A next-generation sequencing approach to river biomonitoring using benthic diatoms. Freshw. Sci. 33:349-363.   DOI
57 Kermarrec, L., Franc, A., Rimet, F., Chaumeil, P., Humbert, J. F. & Bouchez, A. 2013. Next-generation sequencing to inventory taxonomic diversity in eukaryotic communities: a test for freshwater diatoms. Mol. Ecol. Resour. 13:607-619.   DOI
58 Lee, H. Y. 2013. Diversity and biomass of benthic diatoms in Hampyeong Bay tidal flats. Korean J. Environ. Biol. 31:295-301.   DOI
59 Kim, J. -H. & Cho, K. -J. 1985. The physico-chemical properties of sediment, the species composition and biomass of benthic diatoms in the intertidal zone of Kum River estuary. Korean J. Ecol. 8:21-29.
60 Kwon, H. K., Yang, H. S., Yu, Y. M. & Oh, S. J. 2012. Effects of substrate size on the growth of 4 microphytobenthos species (Achnanthes sp., Amphora sp., Navicula sp. and Nitzschia sp.). J. Environ. Sci. 21:105-111.
61 Letunic, I. & Bork, P. 2007. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.   DOI
62 Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S., Jobb, G., Forster, W., Brettske, I., Gerber, S., Ginhart, A. W., Gross, O., Grumann, S., Hermann, S., Jost, R., Konig, A., Liss, T., Lussmann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A. & Schleifer, K. H. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.   DOI
63 MacGillivary, M. L. & Kaczmarska, I. 2011. Survey of the efficacy of a short fragment of the rbcL gene as a supplemental DNA barcode for diatoms. J. Eukaryot. Microbiol. 58:529-536.   DOI
64 Mann, D. G., Sato, S., Trobajo, R., Vanormelingen, P. & Souffreau, C. 2010. DNA barcoding for species identification and discovery in diatoms. Cryptogam. Algol. 31:557-577.
65 Mann, D. G. & Vanormelingen, P. 2013. An inordinate fondness? The number, distributions, and origins of diatom species. J. Eukaryot. Microbiol. 60:414-420.   DOI
66 Kim, D. & Kim, K. H. 2008. Tidal and seasonal variations of nutrients in Keunso Bay, the Yellow Sea. Ocean Polar Res. 30:1-10.
67 Meadows, P. S. & Anderson, J. G. 1968. Micro-organisms attached to marine sand grains. J. Mar. Biol. Assoc. U. K. 48:161-175.   DOI