Skip to main content
Springer Nature Link
Log in

Cell-bound exopolysaccharides from an axenic culture of the intertidal mudflat Navicula phyllepta diatom affect biofilm formation by benthic bacteria

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

Abstract

At low tide, intertidal mudflat biofilms cover large surfaces and are mainly responsible for the high productivity of these marine areas. In the European Atlantic coast, such biofilms are mainly composed of diatoms, especially Navicula phyllepta, bacteria, and microbial extracellular polymeric substances (EPS). To better understand interactions occurring between microorganisms, we first axenized a N. phyllepta culture with a new and simple protocol. Colloidal and bound EPS secreted by diatom cells during the exponential growth and the stationary phase were then harvested, and we tested their effects on the in vitro formation of biofilms by three marine bacteria. The latter had been isolated from a French Atlantic intertidal mudflat and were previously selected for their strong in vitro biofilm-forming ability. They belong to the Flavobacterium, Roseobacter, and Shewanella genera. Navicula phyllepta-bound EPS synthesized during the stationary phase specifically inhibited the biofilm formation by the Flavobacterium sp. strain, whereas they stimulated biofilm development by the two other strains. The EPS acted in all cases during the first stages of the biofilm establishment. Saccharidic molecules were found to be responsible for these activities. This is the first report on marine bacterial antibiofilm saccharides of microalgal origin. This work points out the complexity of the benthic natural biofilms with specific microalgae/bacteria interactions and underlines the possibility to use axenic diatoms as a source of bioactive compounds.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Admiraal W, Peletier H, Brouwer T (1984) The seasonal succession patterns of diatom species on an intertidal mudflat—an experimental analysis. Oikos 42:30–40

    Article  Google Scholar 

  • Amin SA, Parker M, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babor K, Kaláč V, Tihlárik K (1973) Periodate oxidation of saccharides. III. Comparison of the methods for determining the consumption of sodium periodate and the amount of formic acid formed. Chem Zvesti 27:676–680

    CAS  Google Scholar 

  • Basson A, Flemming LA, Chenia HY (2008) Evaluation of adherence, hydrophobicity, aggregation, and biofilm development of Flavobacterium johnsoniae-like isolates. Microb Ecol 55:1–14

    Article  CAS  PubMed  Google Scholar 

  • Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, Orth RJ, Sheridan PF, Weinstein MP (2001) The identification, conservation and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51:633–641

    Article  Google Scholar 

  • Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277

    Article  Google Scholar 

  • Bellinger B, Underwood G, Ziegler S, Gretz M (2009) Significance of diatom-derived polymers in carbon flowdynamics within estuarine biofilms determined through isotopic enrichment. Aquat Microb Ecol 55:169–187

    Article  Google Scholar 

  • Bendaoud M, Vinogradov E, Balashova NV, Kadouri DE, Kachlany SC, Kaplan JB (2011) Broad-spectrum biofilm inhibition by Kingella kingae exopolysaccharide. J Bacteriol 193:3879–3886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruckner CG, Kroth PG (2009) Protocols for the removal of bacteria from freshwater benthic diatom cultures. J Phycol 45:981–986

    Article  CAS  PubMed  Google Scholar 

  • Bruckner CG, Bahulikar R, Rahalkar M, Schink B, Kroth PG (2008) Bacteria associated with benthic diatoms from Lake Constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances. Appl Environ Microbiol 74:7740–7749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruckner CG, Rehm C, Grossart HP, Kroth PG (2011) Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria. Environ Microbiol 13:1052–1063

    Article  CAS  PubMed  Google Scholar 

  • Cammen L (1991) Annual bacterial production in relation to benthic microalgal production and sediment oxygen uptake in an intertidal sandflat and an intertidal mudflat. Mar Ecol Prog Ser 71:13–25

    Article  Google Scholar 

  • Colijn F (1982) Light absorption in the waters of the Ems-Dollard estuary and its consequences for the growth of phytoplankton and microphytobenthos. Neth J Sea Res 15:196–216

    Article  Google Scholar 

  • Consalvey M, Paterson DM, Underwood GJC (2004) The ups and downs of life in a benthic biofilm: migration of benthic diatoms. Diatom Res 19:181–202

    Article  Google Scholar 

  • Cook PLM, Veuger B, Böer S, Middelburg JJ (2007) Effect of nutrient availability on carbon and nitrogen incorporation and flows through benthic algae and bacteria in near-shore sandy sediment. Aquat Microb Ecol 49:165–180

    Article  Google Scholar 

  • da Silva ML, de Oliveira da Rocha FA, Odebrecht C, Giroldo D, Abreu PC (2016) Carbohydrates produced in batch cultures of the surf zone diatom Asterionellopsis glacialis Sensu Lato: influence in vertical migration of the microalga and in bacterial abundance. J Exp Mar Biol Ecol 474:126–132

    Article  Google Scholar 

  • Dang H, Lovell CR (2000) Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 66:467–475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Jonge VN, Colijn F (1994) Dynamics of microphytobenthos biomass in the ems estuary. Mar Ecol Prog Ser 104:185–196

    Article  Google Scholar 

  • Decho AW (2000) Microbial biofilms in intertidal systems: an overview. Continental Shelf Res 20:1257–1273

    Article  Google Scholar 

  • Doghri I, Rodrigues S, Bazire A, Dufour A, Akbar D, Sopena V, Sablé S, Lanneluc I (2015) Marine bacteria from the French Atlantic coast displaying high forming-biofilm abilities and different biofilm 3D architectures. BMC Microbiol 15:231

    Article  PubMed  PubMed Central  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Duchaud E, Boussaha M, Loux V, Bernardet JF, Michel C, Kerouault B, Mondot S, Nicolas P, Bossy R, Caron C, Bessières P, Gibrat JF, Claverol S, Dumetz F, Le Hénaff M, Benmansour A (2007) Complete genome sequence of the fish pathogen Flavobacterium psychrophilum. Nat Biotech 25:763–769

    Article  CAS  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  • Fu W, Wichuk K, Brynjólfsson S (2015) Developing diatoms for value-added products: challenges and opportunities. Nat Biotech 32:547–551

    CAS  Google Scholar 

  • Gärdes A, Iversen MH, Grossart H-P, Passow U, Ullrich MS (2011) Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii. ISME J 5:436–445

    Article  PubMed  Google Scholar 

  • Gontang EA, Fenical W, Jensen PR (2007) Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73:3272–3282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goto N, Mitamura O, Terai H (2001) Biodegradation of photosynthetically produced extracellular organic carbon from intertidal benthic algae. J Exp Mar Biol Ecol 257:73–86

    Article  CAS  PubMed  Google Scholar 

  • Grossart HP, Czub G, Simon M (2006) Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environ Microbiol 8:1074–1084

    Article  PubMed  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervaceae (Cleve) Gran. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Hamels I, Muylaert K, Casteleyn G, Vyverman W (2001) Uncoupling of bacterial production and flagellate grazing in aquatic sediments: a case study from an intertidal flat. Aquat Microb Ecol 25:31–42

    Article  Google Scholar 

  • Haubois AG, Sylvestre F, Guarini JM, Richard P, Blanchard GF (2005) Spatio-temporal structure of the epipelic diatom assemblage from an intertidal mudflat in Marennes-Oléron Bay, France. Estuar Coast Shelf S 64:385–394

    Article  Google Scholar 

  • Haynes K, Hofmann TA, Smith CJ, Ball AS, Underwood GJC, Osborn AM (2007) Diatom-derived carbohydrates as factors affecting bacterial community composition in estuarine sediments. Appl Environ Microbiol 73:6112–6124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersbøll BK, Molin S (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395–2407

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey SW, Humphrey GR (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    Article  CAS  Google Scholar 

  • Jiang P, Li J, Han F, Duan G, Lu X, Gu Y, Yu W (2011) Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLoS One 6:e18514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones PR, Cottrell M, Kirchman DL, Dexter SC (2006) Bacterial community structure of biofilms on artificial surfaces in an estuary. Microb Ecol 53:153–162

    Article  PubMed  Google Scholar 

  • Khandeparker L, DeCosta PM, Anil AC, Sawant SS (2014) Interactions of bacteria with diatoms: influence on natural marine biofilms. Mar Ecol 35:233–248

    Article  CAS  Google Scholar 

  • Kim Y, Oh S, Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun 379:324–329

    Article  CAS  PubMed  Google Scholar 

  • Lavergne C, Beaugeard L, Dupuy C, Courties C, Agogué H (2014) An efficient and rapid method for the enumeration of heterotrophic prokaryotes in coastal sediments by flow cytometry. J Microbiol Meth 105:31–38

    Article  CAS  Google Scholar 

  • Lebeau TL, Robert JMR (2003) Diatom cultivation and biotechnologically relevant products. II. Current and putative products. Appl Microbiol Biotechnol 60:624–632

    Article  CAS  PubMed  Google Scholar 

  • Lee JB, Hayashi K, Hirata M, Kuroda E, Suzuki E, Kubo Y, Hayashi T (2006) Antiviral sulfated polysaccharide from Navicula directa, a diatom collected from deep-sea water in Toyama Bay. Biol Pharm Bull 29:2135–2139

    Article  CAS  PubMed  Google Scholar 

  • Lee JW, Nam JH, Kim YH, Lee KH, Lee DH (2008) Bacterial communities in the initial stage of marine biofilm formation on artificial surfaces. J Microbiol 46:174–182

    Article  CAS  PubMed  Google Scholar 

  • Loke MF, Lui SY, Ng BL, Gong M, Ho B (2007) Antiadhesive property of microalgal polysaccharide extract on the binding of Helicobacter pylori to gastric mucin. FEMS Immunol Med Microbiol 50:231–238

    Article  CAS  PubMed  Google Scholar 

  • Lubarsky HV, Hubas C, Chocholek M, Larson F, Manz W, Paterson DM, Gerbersdorf SU (2010) The stabilisation potential of individual and mixed assemblages of natural bacteria and microalgae. PLoS One 5:e13794

    Article  PubMed  PubMed Central  Google Scholar 

  • Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, Laufs R (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178:175–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Méléder V, Barillé L, Rincé Y, Morançais M, Rosa P, Gaudin P (2005) Spatio-temporal changes in microphytobenthos structure analysed by pigment composition in a macrotidal flat (Bourgneuf Bay, France). Mar Ecol Prog Ser 297:83–99

    Article  Google Scholar 

  • Middelburg JJ, Barranguet C, Boschker HTS, Herman PMJ, Moens T, Heip CHR (2000) The fate of intertidal microphytobenthos carbon: an in situ 13C-labeling study. Limnol Oceanogr 45:1224–1234

    Article  CAS  Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79

    Article  PubMed  Google Scholar 

  • Orvain F, De Crignis M, Guizien K, Lefebvre S, Mallet C, Takahashi E, Dupuy C (2014) Tidal and seasonal effects on the short-term temporal patterns of bacteria, microphytobenthos and exopolymers in natural intertidal biofilms (Brouage, France). J Sea Res 92:6–18

    Article  Google Scholar 

  • Pamp SJ, Sternberg C, Tolker-Nielsen T (2009) Insight into the microbial multicellular lifestyle via flow-cell technology and confocal microscopy. Cytometry A 75:90–103

    Article  PubMed  Google Scholar 

  • Pascal PY, Dupuy C, Richard P, Mallet C, Châtelet EAD, Niquil N (2009) Seasonal variation in consumption of benthic bacteria by meio- and macrofauna in an intertidal mudflat. Limnol Oceanogr 54:1048–1059

    Article  CAS  Google Scholar 

  • Pierre G, Graber M, Rafiliposon B, Dupuy C, Orvain F, Crignis M, Maugard T (2012) Biochemical composition and changes of extracellular polysaccharides (ECPS) produced during microphytobenthic biofilm development (Marennes-Oléron, France). Microb Ecol 63:157–169

    Article  CAS  PubMed  Google Scholar 

  • Pitts B, Hamiltonb MA, Zelverc N, Stewart SS (2003) A microtiter-plate screening method for biofilm disinfection and removal. J Microbiol Meth 54:269–276

    Article  CAS  Google Scholar 

  • Qin Z, Yang L, Qu D, Molin S, Tolker-Nielsen T (2009) Pseudomonas aeruginosa extracellular products inhibit staphylococcal growth, and disrupt established biofilms produced by Staphylococcus epidermidis. Microbiology 155:2148–2156

    Article  CAS  PubMed  Google Scholar 

  • Rendueles O, Travier L, Latour-Lambert P, Fontaine T, Magnus J, Denamur E, Ghigo JM (2011) Screening of Escherichia coli species biodiversity reveals new biofilm-associated anti-adhesion polysaccharides. mBio 2(3):e00043–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Rendueles O, Kaplan JB, Ghigo JM (2013) Antibiofilm polysaccharides. Environ Microbiol 15:334–346

    Article  CAS  PubMed  Google Scholar 

  • Ribalet F, Intertaglia L, Lebaron P, Casotti R (2008) Differential effect of three polyunsaturated aldehydes on marine bacterial isolates. Aquat Toxicol 86:249–255

    Article  CAS  PubMed  Google Scholar 

  • Sablé S, Pons AM, Gendron-Gaillard S, Cottenceau G (2000) Antibacterial activity evaluation of microcin J25 against diarrheagenic Escherichia coli. Appl Environ Microbiol 66:4595–4597

    Article  PubMed  PubMed Central  Google Scholar 

  • Salta M, Wharton JA, Blache Y, Stokes KR, Briand JF (2013) Marine biofilms on artificial surfaces: structure and dynamics. Environ Microbiol 15:2879–2893

    PubMed  Google Scholar 

  • Sayem SA, Manzo E, Ciavatta L, Tramice A, Cordone A, Zanfardino A, De Felice M, Varcamonti M (2011) Antibiofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microb Cell Factories 10:74

    Article  Google Scholar 

  • Schäfer H, Abbas B, Witte H, Muyzer G (2002) Genetic diversity of “satellite” bacteria present in cultures of marine diatoms. FEMS Microbiol Ecol 42:25–35

    PubMed  Google Scholar 

  • Scholz B (2014) Effects of varying pH on the growth and physiology of five marine microphytobenthic diatoms isolated from the Solthörn tidal flat (southern North Sea, Germany). Phycologia 53:252–264

    Article  CAS  Google Scholar 

  • Serôdio J, da Silva JM, Catarino F (1997) Nondestructive tracing of migratory rhythms of intertidal benthic microalgae using in vivo chlorophyll a fluorescence. J Phycol 33:542–553

    Article  Google Scholar 

  • Shishlyannikov SM, Zakharova YR, Volokitina NA, Mikhailov IS, Petrova DP, Likhoshway YV (2011) A procedure for establishing an axenic culture of the diatom Synedra acus subsp. radians (Kütz.) Skabibitsch from Lake Baikal. Limnol Oceanogr Methods 9:478–484

    Article  CAS  Google Scholar 

  • Smith DJ, Underwood GJC (2000) The production of extracellular carbohydrates by estuarine benthic diatoms: the effects of growth phase and light and dark treatment. J Phycol 36:321–333

    Article  CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Staats N, de Winder B, Stal LJ, Mur LR (1999) Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum. Eur J Phycol 34:161–169

    Article  Google Scholar 

  • Takahashi E, Ledauphin J, Goux D, Orvain F (2009) Optimising extraction of extracellular polymeric substances (EPS) from benthic diatoms: comparison of the efficiency of six EPS extraction methods. Mar Freshwat Res 60:1201–1210

    Article  CAS  Google Scholar 

  • Underwood G, Kronkamp R (1999) Primary production by phytoplankton and microphytobenthos in estuaries. Adv Ecol Res 29:93–153

    Article  CAS  Google Scholar 

  • Underwood G, Paterson D (2003) The importance of extracellular carbohydrate production by marine epipelic diatoms. Adv Bot Res 40:183–240

    Article  CAS  Google Scholar 

  • Underwood GJC, Paterson DM, Parkes RJ (1995) The measurement of microbial carbohydrate exopolymers from intertidal sediments. Limnol Oceanogr 40:1243–1253

    Article  CAS  Google Scholar 

  • Underwood GJC, Boulcott M, Raines CA (2004) Environmental effects on exopolymer production by marine benthic diatoms: dynamic, changes in composition, and pathways of production. J Phycol 40:293–301

    Article  CAS  Google Scholar 

  • Urakawa H, Yoshida T, Nishimura M, Ohwada K (2000) Characterization of depth-related population variation in microbial communities of a coastal marine sediment using 16S rDNA-based approaches and quinone profiling. Environ Microbiol 2:542–554

    Article  CAS  PubMed  Google Scholar 

  • Valle J, Da Re S, Henry N, Fontaine T, Balestrino D, Latour-Lambert P, Ghigo JM (2006) Broad spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci U S A 103:12558–12563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Duyl FC, de Winder B, Kop AJ, Wollenzien U (1999) Tidal coupling between carbohydrate concentrations and bacterial activities in diatom-inhabited intertidal mudflats. Mar Ecol Prog Ser 191:19–32

    Article  Google Scholar 

  • van Duyl FC, Winder BD, Kop AJ, Wollenzien U (2000) Consequences of diatom mat erosion for carbohydrate concentrations and heterotrophic bacterial activities in intertidal sediments of the Ems-Dollard estuary. Cont Shelf Res 20:1335–1349

    Article  Google Scholar 

  • Windler M, Gruber A, Kroth PG (2012) Technical note: purification of benthic diatoms from associated bacteria using the antibiotic imipenem. J Endocytobiosis Cell Res 62–65

  • Windler M, Leinweber K, Bartulos CR (2015) Biofilm and capsule formation of the diatom Achnanthidium minutissimum are affected by a bacterium. J Phycol 51:343–355

    Article  CAS  PubMed  Google Scholar 

  • Yu X, He W, Li H, Yan Y, Lin C (2010) Larval settlement and metamorphosis of the pearl oyster Pinctada fucata in response to biofilms. Aquaculture 306:334–337

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank the Conseil Général de la Charente Maritime (France) for the Ph.D. grant of Ibtissem Doghri, the CPER littoral 2007-14 (France), the CNRS EC2CO program MicroBiEn 2013-14 (France), the Région Poitou-Charente (France) and the Région Bretagne (France), and the European FEDER funds, for their financial support.

Author information

Author notes

  1. Johann Lavaud

    Present address: UMI 3376 TAKUVIK, Département de Biologie, CNRS-Université Laval, Pavillon Alexandre-Vachon, 1045 avenue de la Médecine, Québec, G1V 0A6, Canada

Authors and Affiliations

  1. LIENSs, UMR 7266 Université de La Rochelle-CNRS, Univ. La Rochelle, F-17042, La Rochelle Cedex 01, France

    Ibtissem Doghri, Johann Lavaud, Isabelle Lanneluc & Sophie Sablé

  2. EA 3884, LBCM, IUEM, Univ. Bretagne-Sud, F-56100, Lorient, France

    Alain Dufour & Alexis Bazire

Authors
  1. Ibtissem Doghri
    View author publications

    Search author on:PubMed Google Scholar

  2. Johann Lavaud
    View author publications

    Search author on:PubMed Google Scholar

  3. Alain Dufour
    View author publications

    Search author on:PubMed Google Scholar

  4. Alexis Bazire
    View author publications

    Search author on:PubMed Google Scholar

  5. Isabelle Lanneluc
    View author publications

    Search author on:PubMed Google Scholar

  6. Sophie Sablé
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Lanneluc.

Additional information

Isabelle Lanneluc and Sophie Sablé contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Doghri, I., Lavaud, J., Dufour, A. et al. Cell-bound exopolysaccharides from an axenic culture of the intertidal mudflat Navicula phyllepta diatom affect biofilm formation by benthic bacteria. J Appl Phycol 29, 165–177 (2017). https://doi.org/10.1007/s10811-016-0943-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0943-z

Keywords