Skip to main content

Advertisement

SpringerLink
Log in

Variation in “bank of microscopic forms” in urchin barren coast: detection using DNA metabarcoding based on high-throughput sequencing

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Type of macroalgal beds that recovered from sea urchin barrens is determined by components of “bank of microscopic forms.” In the present study, we investigated the variation of the bank components, especially in the Phaeophyceae and Rhodophyta, on cobbles at four different vegetation and depths (1, 2, 5, and 7 m) of urchin barren grounds (UB1, UB2, UB5, and UB7), and alternative ecological phases (EB, ecklonian kelp bed and SC, soft coral bed). We collected 30 cobbles (3–7 cobbles per station) from the six stations and identified the attached algae by DNA metabarcoding based on high-throughput sequencing. In the rarefied data, 74 macroalgal operational taxonomic units (OTUs) were detected, of which 32 and 42 OTUs were assigned to Phaeophyceae and Rhodophyta, respectively. The OTU richness in urchin barrens increased with depth from UB1 (0.07 ± 0.03 OTUs cm−2 of cobble) to UB7 (0.21 ± 0.12 OTUs cm−2 of cobble), which was similar to the other ecological phases (EB and SC). The Shannon-Weiner diversity index in UB7 was also significantly highest and similar to EB and SC (p < 0.05). However, the ordination test (non-metric multidimensional scaling) assigned EB to different group apart from UB7 and SC, probably due to solely Phaeophyceae dominance in EB. Therefore, macroalgal richness and components of the bank could be determined by depth and ecological phases, respectively. Furthermore, OTU identified as Undaria pinnatifida was detected on a cobble collected UB7. Thus, in urchin barren coast, the richness in kelp gametophyte is probably also higher in deeper area.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akita S, Takano Y, Nagai S, Kuwahara H, Kajihara R, Tanabe AS, Fujita D (2019) Rapid detection of bank of microscopic form on cobbles: application of DNA metabarcoding using next-generation sequencing. J Appl Phycol 31:2743–2753

    CAS  Google Scholar 

  • Akita S, Yamada H, Ito M, Kobayashi M, Fujita D (2014) Phenology of annual kelp Eckloniopsis (Phaeophyceae, Laminariales) forest on a Diadema barren in Uchiura Bay, Central Pacific Coast of Honshu, Japan. J Appl Phycol 26:1141–1148

  • Akita S, Yamada H, Ito M, Graham MH, Fujita D (2016) Sorus formation on the holdfast haptera of the kelp Ecklonia radicosa (Phaeophyceae, Laminariales). Bot Mar 59:433–438

    Google Scholar 

  • Amsler CD, Searles RB (1980) Vertical distribution of seaweed spores in a water column offshore of North Carolina. J Phycol 16:617–619

    Google Scholar 

  • Burrows EM (1958) Subtidal algal population in Port Erin Bay, Isle of Man. J Mar Biol Assoc UK 37:687–703

    Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL et al (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421

    PubMed  PubMed Central  Google Scholar 

  • Dayton PK (1985) Ecology of kelp communities. Annu Rev Ecol Syst 16:215–245

    Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards MS (2000) The role of alternate life-history stages of a marine macroalga: a seed bank analogue? Ecology 81:2404–2415

    Google Scholar 

  • Engelen AH, Lévèque L, Destombe C, Valero M (2011) Spatial and temporal patterns of recovery of low intertidal Laminaria digitata after experimental spring and autumn removal. Cah Biol Mar 52:441–453

    Google Scholar 

  • Filbee-Dexter K, Scheibling RE (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar Ecol Prog Ser 495:1–25

    Google Scholar 

  • Fox CH, Swanson AK (2007) Nested PCR detection of microscopic life-stages of laminarian macroalgae and comparison with adult forms along intertidal height gradients. Mar Ecol Prog Ser 332:1–10

    CAS  Google Scholar 

  • Fredericq S, Krayesky-Self S, Sauvage T, Richards J, Kittle R, Arakaki N, Hicherson E, Schmidt WE et al (2019) The critical importance of rhodoliths in the life cycle completion of both macro- and microalgae, and as holobionts for the establishment and maintenance of marine biodiversity. Front Mar Sci 5:502

    Google Scholar 

  • Fujita D (2003) Algal recovery urchin-dominated on coralline-covered cobbles collected from urchin-dominated barren ground in flowing deep-sea water II. Deep Ocean Water Res 4:1–9 (in Japanese with English abstract)

    Google Scholar 

  • Fujita D (2004) Nutrients and snail grazing affect recovery of algal vegetation on cobbles transplanted from a barren ground in southwestern Hokkaido to aquaria. Jap J Phycol (Sorui) 52:23–32

    Google Scholar 

  • Gentleman R, Carey V, Huber W, Hahne F (2018) Genefilter: methods for filtering genes from high-throughput experiments R package version 1.64.0. Available here: https://bioconductor.org/packages/release/bioc/html/genefilter.html. Accessed June 2018

  • Graham MH (2004) Effects of local deforestation on the diversity and structure of southern California giant kelp forest food webs. Ecosystems 7:341–357

    Google Scholar 

  • Guiry MD, Guiry GM (2016) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; Accessed on July 2016

  • Hayakawa Y, Kawata K, Machida K, Yamano S, Akita S, Fijita D (2017) Phenology of Chondracanthus tenellus (Rhodophyta) in the central Pacific coast of Honshu, Japan. J Appl Phycol 29:2547–2556

    Google Scholar 

  • Hoffmann AJ, Avila M, Santelices B (1984) Interactions of nitrate and phosphate on the development of microscopic stages of Lessonia nigrescens Bory (Phaeophyceae). J Exp Mar Biol Ecol 78:177–186

    CAS  Google Scholar 

  • Hoffmann AJ, Camus P (1989) Sinking rates and viability of spores from benthic algae in central Chile. J Exp Mar Biol Ecol 126:281–291

    Google Scholar 

  • Hoffmann AJ, Santelices B (1991) Banks of algal microscopic forms: hypotheses on their functioning and comparisons with seed banks. Marine ecology progress series. Mar Ecol Prog Ser 79:185–194

    Google Scholar 

  • Kain JM (1964) Aspects of the biology of Laminaria hyperborea. III. Survival and growth of gametophytes. J Mar Biol Assoc UK 44:415–433

    Google Scholar 

  • Kobayashi M, Fujita D (2014) Can thallus color of red algae be used as an environmental indicator in shallow waters? J Appl Phycol 26:1123–1131

    CAS  Google Scholar 

  • Ladah LB, Zertuche–González JA, Hernández–Carmona G (1999) Giant kelp (Macrocystis pyrifera, Phaeophyceae) recruitment near its southern limit in Baja California after mass disappearance during ENSO 1997–1998. J Phycol 35:1106–1112

    Google Scholar 

  • Leliaert F, Verbruggen H, Vanormelingen P, Steen F, Lopez-Bautista JM, Zuccharello GC, De Clerck O (2014) DNA-based species delimitation in algae. Eur J Phycol 49:179–196

  • Lieberman M, John DM, Lieberman D (1979) Ecology of subtidal algae on seasonally devastated cobble substrates off Ghana. Ecology 60:1151–1161

    Google Scholar 

  • Ling SD, Scheibling RE, Rassweiler A, Johnson CR, Shears N, Connell SD, Salomon AK, Norderhaug KM, Pérez-Matus A, Hernández JC, Clemente S, Blamey LK, Hereu B, Ballesteros E, Sala E, Garrabou J, Cebrian E, Zabala M, Fujita D, Johnson LE (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos Trans R Soc B 370:20130269

    Google Scholar 

  • Marcelino VR, Verbruggen H (2016) Multi-marker metabarcoding of coral skeletons reveals a rich microbiome and diverse evolutionary origins of endolithic algae. Sci Rep 6:31508

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nanri K, Nakajima Y, Yatsuya K, Kiyomoto S, Andou W, Yoshimura T (2011) Some approaches for the recovery from barren ground in Shin-Mie, Nagasaki prefecture. J Fish Engr 48:59–64 (Japanese with English abstract)

    Google Scholar 

  • Neushul M, Dahl AL (1967) Composition and growth of subtidal parvosilvosa from Californian kelp forests. Helgol Wiss Meeresunters 15:480–488

    Google Scholar 

  • Nishitani G, Nagai S, Hayakawa S, Kosaka Y, Sakurada K, Kamiyama T, Gojobori T (2012) Multiple plastids collected by the dinoflagellate Dinophysis mitra through kleptoplastidy. Appl Environ Microbiol 78:813–821

    CAS  PubMed  PubMed Central  Google Scholar 

  • North WJ (1971) The biology of giant kelp beds (Macrocystis) in California: introduction and background. Nova Hedwigia 32:1–68

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R et al (2015) vegan: community ecology package. R package vegan, vers. 2.2-1. Available here: https://cran.r-project.org/web/packages/vegan/index.html. Accessed June 2015

  • Okuda T, Neushul M (1981) Sedimentation studies of red algal spores. J Phycol 17:113–118

    Google Scholar 

  • Pavan-Kumar A, Gireesh-Babu P, Lakra WS (2015) DNA metabarcoding: a new approach for rapid biodiversity assessment. J Cell Sci Mol Biol 2:111

    Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Accessed June 2015

  • Santelices B, Hoffmann AJ, Aedo D, De Bobadilla MF, Otaiza R et al (1995) A bank of microscopic forms on disturbed boulders and stones in tide pools. Mar Ecol Prog Ser 129:215–228

    Google Scholar 

  • Sauvage T, Schmidt WE, Suda S, Fredericq S (2016) A metabarcoding framework for facilitated survey of endolithic phototrophs with tufA. BMC Ecol 16:8

    PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sherwood AR, Dittbern MN, Johnston ET, Conklin KY (2017) A metabarcoding comparison of windward and leeward airborne algal diversity across the Ko‘olau mountain range on the island of O‘ahu, Hawaii. J Phycol 53:437–445

    CAS  PubMed  Google Scholar 

  • Shum P, Barney BT, O’Leary JK, Palumbi SR (2019) Cobble community DNA as a tool to monitor patterns of biodiversity within kelp forest ecosystems. Mol Ecol Resour 19:1470–1485

    CAS  PubMed  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459

    Google Scholar 

  • Steneck RS, Johnson C (2014) Kelp forests: dynamic patterns, processes and feedbacks. In: Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) Marine community ecology and conservation. Sinauer Associates, Sunderland, pp 315–366

    Google Scholar 

  • Tanabe AS (2012) ASSAMS v0.1.2013.07.19. Available here: http://www.fifthdimension.jp/. Accessed June 2015

  • Tanabe AS, Nagai S, Hida K, Yasuike M, Fujiwara A, Nakamura Y, Takano Y, Katakura S (2016) Comparative study of the validity of three regions of the 18S-rRNA gene for massively parallel sequencing-based monitoring of the planktonic eukaryote community. Mol Ecol Resour 16:402–414

    CAS  PubMed  Google Scholar 

  • Toohey BD, Kendrick GA, Harvey ES (2007) Disturbance and reef topography maintain high local diversity in Ecklonia radiata kelp forests. Oikos 116:1618–1630

    Google Scholar 

  • Tsutsui I, Ohno M (1993) Growth and maturation of Undaria pinnatifida, U. undarioides and Eckloniopsis radicosa at Susaki Bay of Kochi in Japan. Aquacult Sci 41:55–60 (Japanese with English abstract)

    Google Scholar 

  • Warnes GR, Bolker B, Bonebakker L et al (2009) gplots: various R programming tools for plotting data. Available here: https://cran.r-project.org/web/packages/gplots/index.html. Acceses June 2015

  • Watanuki A, Aota T, Otsuka E, Kawai T, Iwahashi Y, Kuwahara H, Fujita D (2010) Restoration of kelp beds on an urchin barren: removal of sea urchins by citizen divers in southwestern Hokkaido. Bull Fish Res Agen 32:83–87

    Google Scholar 

  • Worm B, Lotze HK, Boström C, Engkvist R, Labanasukas V, Sommer U (1999) Marine diversity shift linked to interactions among grazers, nutrients and propagule banks. Mar Ecol Prog Ser 185:309–314

    Google Scholar 

  • Worm B, Lotze HK, Sommer U (2001) Algal propagule banks modify competition, consumer and resource control on Baltic rocky shores. Oecologia 128:281–293

    PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Tatsuru Kadota, Mr. Taku Yoshimura, and the local fishermen for their assistance during the survey. We would like to thank Editage for English language editing.

Funding

This work was supported by a research project grant from the Fisheries Research Agency of Japan (FRA) to SN and JSPS KAKENHI (grant no. 15K07525) to DF.

Author information

Author notes

  1. Shingo Akita

    Present address: Faculty of Core Research, Natural Science Division, Ochanomizu University, 2-1-1 Otsuka, Bunkyo-ku, Tokyo, 112-8610, Japan

  2. Yoshihito Takano

    Present address: Faculty of Science and Technology, Kochi University, 200 Monobe, Nankoku, 783-8502, Kochi, Japan

Authors and Affiliations

  1. Laboratory of Applied Phycology, Graduate School of Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo, 108-8477, Japan

    Shingo Akita, Hiroki Murasawa & Daisuke Fujita

  2. National Research Institute of Fisheries Science, 2-12-4 Fukuura, Kanazawa-ku, Yokohama, 236-8648, Kanagawa, Japan

    Yoshihito Takano & Satoshi Nagai

  3. AXIOHELIX Co. Ltd., Nihonbashi, Chuo-ku, Tokyo, 103-0015, Japan

    Yoko Kawakami

Authors
  1. Shingo Akita
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroki Murasawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoshihito Takano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoko Kawakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daisuke Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Satoshi Nagai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shingo Akita.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 6560 kb)

ESM 2

(DOCX 17 kb)

ESM 3

(XLSX 49 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akita, S., Murasawa, H., Takano, Y. et al. Variation in “bank of microscopic forms” in urchin barren coast: detection using DNA metabarcoding based on high-throughput sequencing. J Appl Phycol 32, 2115–2124 (2020). https://doi.org/10.1007/s10811-020-02122-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02122-3

Keywords

Search

Navigation