Review
Seawater at the nanoscale: marine gel imaged by atomic force microscopy†
Tea Mišić Radić,
Vesna Svetličić,
Vera Žutić,
Beate Boulgaropoulos,
Corresponding Author
Tea Mišić Radić
Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička 54, 10000 Zagreb, Croatia
Division for Marine and Environmental Research, Ruder Boskovic Institute, Bijenicka 54, 10000 Zagreb, Croatia.Search for more papers by this authorVesna Svetličić
Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička 54, 10000 Zagreb, Croatia
Search for more papers by this authorVera Žutić
Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička 54, 10000 Zagreb, Croatia
Search for more papers by this authorBeate Boulgaropoulos
Institute of Biophysics and Nanosystems Research, Austrian Academy of Sciences, Schmiedlstraße 6, 8042 Graz, Austria
Search for more papers by this authorTea Mišić Radić,
Vesna Svetličić,
Vera Žutić,
Beate Boulgaropoulos,
Corresponding Author
Tea Mišić Radić
Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička 54, 10000 Zagreb, Croatia
Division for Marine and Environmental Research, Ruder Boskovic Institute, Bijenicka 54, 10000 Zagreb, Croatia.Search for more papers by this authorVesna Svetličić
Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička 54, 10000 Zagreb, Croatia
Search for more papers by this authorVera Žutić
Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička 54, 10000 Zagreb, Croatia
Search for more papers by this authorBeate Boulgaropoulos
Institute of Biophysics and Nanosystems Research, Austrian Academy of Sciences, Schmiedlstraße 6, 8042 Graz, Austria
Search for more papers by this author†
This article is published in Journal of Molecular Recognition as a focus on AFM on Life Sciences and Medicine, edited by Jean-Luc Pellequer and Pierre Parot (CEA Marcoule, Life Science Division, Bagnols sur Cèze, France).
Abstract
The present study introduces atomic force microscopy (AFM) as a tool for characterization of marine gel network and marine biopolymers self-assembly, not accessible by other techniques. AFM imaging of marine gel samples collected in summers 2003 and 2004 in the northern Adriatic Sea provided insight into molecular organization of gel network and associations between polysaccharide fibrils in the network. Initial stages of biopolymers self-assembly were visualized by AFM in a phytoplankton bloom experiment performed in the same aquatorium. Based on AFM imaging and differential scanning calorimetry, the marine gel is characterized as a thermoreversible physical gel and the dominant mode of gelation as crosslinking of polysaccharide fibrils by hydrogen bonding which results in helical structures and their associations. Direct deposition of whole seawater on freshly cleaved mica followed by rinsing was the procedure that caused the least impact on the original structures of biopolymer assemblies in seawater. Copyright © 2011 John Wiley & Sons, Ltd.
REFERENCES
- Abu-Lail NI, Camesano TA. 2003. Polysaccharide properties probed with atomic force microscopy. J. Microsc. 212: 217–238.
- Abu-Lail NI, Camesano TA. 2004. Atomic force microscope and single-molecule force microscopy studies of biopolymers. In Dekker Encyclopedia of Nanoscience and Nanotechnology, J Schwarz, C Contescu, K Putyera (ed.). Taylor & Francis: London; 119–131.
- Baalousha M, Lead JR. 2007. Characterization of natural aquatic colloids (< 5nm) by flow-field flow fractionation and atomic force microscopy. Environ. Sci. Technol. 41: 1111–1117.
- Balnois E, Wilkinson KJ. 2002. Sample preparation techniques for the observation of environmental biopolymers by atomic force microscopy. Colloid Surf. A 207: 229–242.
- Chanzy H, Vuong R. 1985. Ultrastructure and morphology of crystalline polysaccharides. In Polysaccharides: Topics in Structure and Morphology, EDT Atkins (ed.). VCH: Weinheim; 41–71.
10.1007/978-1-349-06369-7_2 Google Scholar
- Chin W-C, Orellana MV, Verdugo P. 1998. Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 391: 568–572.
- CIESM. 2006. Production and fate of dissolved organic matter in the Mediterranean Sea. CIESM Workshop Monographs No. 28, Executive Summary, pp. 5–10.
- Cowman MK, Li M, Balazs EA. 1998. Tapping mode atomic force microscopy of hyaluronan—extended and intramolecularly interacting chains. Biophys. J. 75: 2030–2037.
- Cozzi S, Ivančić I, Catalano G, Đakovac T, Degobbis D. 2004. Dynamics of the oceanographic properties during mucilage appearance in the Northern Adriatic Sea: analysis of the 1997 event in comparison to earlier events. J. Marine Syst. 50: 223–241.
- Đakovac T. 2006. Frequency and conditions during mucilage events, marked hypoxia and anoxia in the northern Adriatic Sea, PhD thesis, University of Zagreb, Zagreb, 139 pp.
- Ding Y-X, Chin W-C, Rodriguez A, Hung C-C, Santschi PH, Verdugo P. 2008. Amphiphilic exopolymers from Sagittula stellata induce DOM self-assembly and formation of marine microgels. Mar. Chem. 112: 11–19.
- Ding Y-X, Chin W-C, Verdugo P. 2007. Development of a fluorescence quenching assay to measure the fraction of organic carbon present in self-assembled gels in seawater. Mar. Chem. 106: 456–462.
- Fonda Umani S, Del Negro P, Larato C, De Vittor C, Cabrini M, Celio M, Falconi C, Tamberlich F, Azam F. 2007. Major inter-annual variations in microbial dynamics in the Gulf of Trieste (northern Adriatic Sea) and their ecosystem implications. Aquat. Microb. Ecol. 46: 163–175.
- Fonda Umani S, Ghirardelli E, Specchi M. 1989. Gli episodi di “mare sporco” nell´ Adriatico dal 1729 ai giorni nostri. Regione Autonoma Friuli Venezia Giulia, Direzione Regionale dell´Ambiente: Trieste.
- Funami T, Hiroe M, Noda S, Asai I, Ikeda S, Nishimari K. 2007. Influence of molecular structure imaged with atomic force microscopy on the rheological behavior of carrageenan aqueous systems in the presence or absence of cations. Food Hydrocolloid 21: 617–629.
- Giani M, Berto D, Zangrando V, Castelli S, Sist P, Urbani R. 2005a. Chemical characterization of different typologies of mucilaginous aggregates in the Northern Adriatic Sea. In: Mucilages in the Adriatic and Tyrrhenian Seas (Giani M Degobbis D and Rinaldi A, eds.) Sci. Total Environ. 353: 232–246.
- Giani M, Degobbis D, Rinaldi A. 2005b (eds.) Mucilages in the Adriatic and Tyrrhenian Seas. Sci. Total Environ. 353: 1–379.
- Giani M, Rinaldi A, Degobbis D. 2005c. Mucilages in the Adriatic and Tyrrhenian Sea: an introduction. In: Mucilages in the Adriatic and Tyrrhenian Seas (GianiM, Degobbis D and Rinaldi A, eds.) Sci. Total Environ. 353: 3–9.
- Iijima M, Hatakeyama T, Takahashi M, Hatakeyama H. 2007. Effect of thermal history on kappa-carrageenan hydrogelation by differential scanning calorimetry. Thermochim. Acta 452: 53–58.
- Ikeda S, Morris VJ, Nishinari K. 2001. Microstructure of aggregated and nonaggregated kappa-carrageenan helices visualized by atomic force microscopy. Biomacromolecules 2: 1331–1337.
- Keresztes Z, Rigó T, Telegdi J, Kálmán E. 2001. Investigation of biopolymer networks by means of AFM. Appl. Phys. A (Suppl.) 72: S113–S116.
- Kirby AR, Gunning AP, Morris VJ. 1996. Imaging polysaccharides by atomic force microscopy. Biopolymers 38: 355–366.
10.1002/(SICI)1097-0282(199603)38:3<355::AID-BIP8>3.0.CO;2-T CAS PubMed Web of Science® Google Scholar
- Kirby AR, Gunning AP, Morris VJ, Ridout MJ. 1995. Observation of the helical structure of the bacterial polysaccharide acetan by atomic force microscopy. Biophys. J. 68: 360–363.
- Kovač N, Bajt O, Faganeli J, Sket B, Orel B. 2002. Study of macroaggregate composition using FT-IR and 1H-NMR spectroscopy. Mar. Chem. 78: 205–215.
- Kovač N, Faganeli J, Bajt O, Sket B, Orel B, Penna N. 2004. Chemical composition of macroaggregates in the northern Adriatic sea. Org. Geochem. 35: 1095–1104.
- Kovač N, Mozetič P, Trichet J, Defarge C. 2005. Phytoplankton composition and organic matter organization of mucous aggregates by means of light and cryo-scanning electron microscopy. Mar. Biol. 147: 261–271.
- Lead JR, Muirhead D, Gibson CT. 2005. Characterization of freshwater natural aquatic colloids by atomic force microscopy (AFM). Environ. Sci. Technol. 39: 6930–6936.
- Leppard GG. 1999. Structure/function/activity relationship in marine snow. Current understanding and suggesting research thrusts. In: State of the art and new scientific hypotheses on the phenomenon of mucilages in the Adriatic Sea (Funari E, Azam F, Fonda Umani S, Pagnotta R, eds.) Ann. Ist. Super. Sanità 35: 389–395.
- Magonov SN. 2000. Atomic force microscopy in analysis of polymers. In Encyclopedia of Analytical Chemistry, RA Meyers (ed.). John Wiley & Sons Ltd: Chichester; 7432–7491.
- Malfatti F, Turk V, Tinta T, Mozetič P, Samo T, Kovač N, Stefanelli M, Manganelli M, Fonda-Umani S, Del Negro P, Caaletto B, Azam F. 2009. Microbial regulation of carbon and phosphorus cycling during a mesocosm phytoplankton bloom in the North Adriatic Sea. 11th Symposium of Aquatic Microbial Ecology, 30 August–3 September 2009, Piran, Slovenia, Abstract book, p.33.
- Mangione MR, Giacomazza D, Bulone D, Martorana V, San Biagio PL. 2003. Thermoreversible gelation of kappa-Carrageenan: relation between conformational transition and aggregation. Biophys. Chem. 104: 95–105.
- McIntire TM, Brant DA. 1997a. Imaging carbohydrate polymers with noncontact mode atomic force microscopy. In Techniques in Glycobiology, RR Townsend, AT Hotchkiss (ed.). Marcel Dekker, Inc.: New York; 187–208.
- McIntire TM, Brant DA. 1997b. Imaging of individual biopolymers and supramolecular assemblies using noncontact atomic force microscopy. Biopolymers 42: 133–146.
10.1002/(SICI)1097-0282(199708)42:2<133::AID-BIP3>3.0.CO;2-O CAS PubMed Web of Science® Google Scholar
- Morris VJ, Kirby AR, Gunning AP. 1999. Atomic Force Microscopy for Biologist. Imperial College Press: London.
10.1142/p173 Google Scholar
- Noda S, Funami T, Nakauma M, Asai I, Takahashi R, Al-Assaf S, Ikeda S, Nishinari K, Phillips GO. 2008. Molecular structures of gellan gum imaged with atomic force microscopy in relation to the rheological behavior in aqueous systems. 1. Gellan gum with various acyl contents in the presence and absence of potassium. Food Hydrocolloid 22: 1148–1159.
- Nunez-Santiago MD, Tecante A. 2007. Rheological and calorimetric study of the sol-gel transition of kappa-carrageenan. Carbohydr. Polym. 69: 763–773.
- Orellana MV, Petersen TW, Diercks AH, Donohoe S, Verdugo P, van den Engh G. 2007. Marine microgels: optical and proteomic fingerprints. Mar. Chem. 105: 229–239.
- Radotić K, Mićić M, Jeremić M. 2006. Scanning probe microscopy of plant cell wall and its constituents. In Force Microscopy: Applications in Biology and Medicine, BP Jena, JKH Hoerber (ed.). John Wiley & Sons, Inc: New York; 95–112.
10.1002/0470007702.ch6 Google Scholar
- Rinaudo M. 2005. Advances in characterization of polysaccharides in aqueous solution and gel state. In Polysaccharides-Structural Diversity and Functional Versatility, S Dumitriu (ed.). Marcel Dekker: New York; 237–252.
- Santschi PH, Balnois E, Wilkinson KJ, Zhang J, Buffle J. 1998. Fibrillar polysaccharides in marine macromolecular organic matter as imaged by atomic force microscopy and transmission electron microscopy. Limnol. Oceanogr. 43: 896–908.
- Schaeffer TE. 2006. High-speed atomic force microscopy of biomolecules in motion. In Force Microscopy: Applications in Biology and Medicine, BP Jena, JKH Hoerber (ed.). John Wiley & Sons. New York; 221–248.
10.1002/0470007702.ch13 Google Scholar
- Stachowitsch M, Fanuko N, Richter M. 1990. Mucous aggregates in the Adriatic Sea: an overview of stages and accourence. P.S.Z.N.I: Mar. Ecol. 11: 327–350.
- Urbani R, Cesaro A. 2001. Chain conformations of polysaccharides in different solvents. In Handbook of Solvents, G Wypych (ed.). ChemTec Publishing: Toronto; 706–735.
- Verdugo P, Alldredge AL, Azam F, Kirchman DL, Passow U, Santschi PH. 2004. The oceanic gel phase: a bridge in the DOM-POM continuum. Mar. Chem. 92: 67–85.
- Verdugo P, Orellana MV, Chin WC, Petersen TW, van den Eng G, Benner R, Hedges JI. 2008. Marine biopolymer self-assembly: implications for carbon cycling in the ocean. Faraday Discuss. 139: 393–398.
- Vollenweider RA, Rinaldi A. 1995. (eds.) Marine mucilages. Sci. Total Environ. 165: 1–235.
- Wells ML. 1998. Marine colloids—a neglected dimension. Nature 391: 530–531.
- Zambianchi E, Calvitti C, Cecamore P, D'Amico F, Ferulano E, Lanciano P. 1992. The mucilage phenomenon in the Northern Adriatic sea, summer 1989: a study carried out with remote sensing techniques. Sci. Total Environ. (Suppl.) 581–598.
- Žutić V, Svetličić V, Radić T, Malfatti F, Degobbis D, Azam F. 2004. Controlled ecosystem carbon flow experiment in the Northern Adriatic Sea. In: Effects of phosphorus on particle dynamics during phytoplankton blooms. Northern Adriatic mesocosm experiment Rovinj 2003 (SmodlakaN, Degobbis D, Svetličić V, eds.) Period. Biol. 106: 1–6.
Citing Literature
