Abstract
The dissolved organic carbon (DOC) depth profiles and the morphology of in-vitro coagulated dissolved organic matter (DOM) were investigated in a steady-state mostly anoxic aquatic system (Lac Pavin monimolimnion). High-resolution cryo-scanning electron microscopy (Cryo-HRSEM) was used to reveal the ultrastructure of the coagulated matter. The study focused on differences in DOC concentrations and coagulation morphotypes between microfiltered and nanofiltered waters. Two types of molecular weight (MW) DOC profiles were identified: although all MW DOC concentrations increased across the chemocline, high MW DOC (> 1 kDa) continued to increase significantly below, while low MW DOC (< 1 kDa) had a quasi-constant value downward the monimolimnion. Cryo-HRSEM images showed organic material composed on the one hand of various distinct shapes such as sheets, nanobelts, tubes, rings, platelets and globules entangled with each other, and on the other hand of fragments of netted threads, trapping Fe-phosphate grains. MW DOC depth profiles and the coagulation morphotype distribution suggest that the distinct organic shapes (sheets, tubes, rings, etc.) correspond to lower MW DOM equally distributed through the monimolimnion, while netted material should be attributed to higher MW DOM scavenged during its upward turbulent diffusion through the monimolimnion. It is concluded that recycling by sedimentation in the monimolimnion does not involve the total DOC but specifically the higher MW DOC imaged by meshed threads coagulated and aggregated in flocculation networks. Ultrastructural 3D morphological observation through Cryo-HRSEM is proposed as a tool to characterize DOM.
Highlights
• Dissolved organic carbon molecular weights are fractionated through the water column.
• 3D Cryo-HRSEM images distinguish different coagulate morphotypes.
• Flocculation limits high molecular weight dissolved organic carbon diffusion.
• Differential nanostructural gelation controls diffusion, flocculation, and sedimentation.
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References
Aeschbach-Hertig W, Hofer M, Schmid M, Kipfer R, Imboden DM (2002) The physical structure and dynamics of a deep, meromictic crater lake (Lac Pavin, France). Hydrobiologia 487:111–136. https://doi.org/10.1023/a:1022942226198
Aiken GR, Hsu-Kim H, Ryan JN (2011) Influence of dissolved organic matter on the environmental fates of metals, nanoparticles, and colloids. Environ Sci Technol 45:3196–3201. https://doi.org/10.1021/es103992s
Albéric P (2011) Liquid chromatography/mass spectrometry stable isotope analysis of dissolved organic carbon in stream and soil waters. Rapid Commun Mass Spectrom 25:3012–3018. https://doi.org/10.1002/rcm.5212
Albéric P, Viollier E, Jézéquel D, Grosbois C, Michard G (2000) Interactions between trace elements and dissolved organic matter in the stagnant anoxic deep layer of a meromictic lake. Limnol Oceanogr 45:1088–1096. https://doi.org/10.4319/lo.2000.45.5.1088
Albéric P, Jézéquel D, Bergonzini L, Chapron E, Viollier E, Massault M, Michard G (2013) Carbon cycling and organic radiocarbon reservoir effect in a meromictic crater lake (Lac Pavin, Puy-de-Dôme, France). Radiocarbon 55:1029–1042. https://doi.org/10.1017/s0033822200058161
Amblard C, Bourdier G (1990) The spring bloom of the diatom Melosira italica ssp. subartica in Lake Pavin: biochemical, energetic and metabolic aspects during sedimentation. J Plankton Res 12:645–660. https://doi.org/10.1093/plankt/12.3.645
Apkarian R (2006) Cryo-temperature stages in nanostructural research. In: Zhou W, Wang ZL (eds) Scanning Microscopy for Nanotechnology. Springer, New York, pp 467–489. https://doi.org/10.1007/978-0-387-39620-0_15
Balistrieri LS, Murray JW, Paul B (1994) The geochemical cycling of trace elements in a biogenic meromictic lake. Geochim Cosmochim Acta 58:3993–4008. https://doi.org/10.1016/0016-7037(94)90262-3
Berg JS, Jézéquel D, Duverger A, Lamy D, Laberty-Robert C, Miot J (2019) Microbial diversity involved in iron and cryptic sulfur cycling in the ferruginous, low-sulfate waters of Lake Pavin. PLoS One 14:e0212787. https://doi.org/10.1371/journal.pone.0212787
Boehrer B, von Rohden C, Schultze M (2017) Physical features of meromictic lakes: Stratification and circulation. In: Gulati R, Zadereev E, Degermendzhi A (eds) Ecology of Meromictic Lakes. Ecological Studies, vol 228. Springer, Cham, pp 15–34. https://doi.org/10.1007/978-3-319-49143-1_2
Bonhomme C, Jézéquel D, Poulin M, Saad M, Vinçon-Leite B, Tassin B (2016) Lake Pavin mixing: New insights from high resolution continuous measurements. In: Sime-Ngando T, Boivin P, Chapron E, Jezequel D, Meybeck M (eds) Lake Pavin. Springer, Cham, pp 177–184. https://doi.org/10.1007/978-3-319-39961-4_10
Buffle J, De Vitre RR, Perret D, Leppard GG (1989) Physico-chemical characteristic of a colloidal iron phosphate species formed at the oxic-anoxic interface of a eutrophic lake. Geochim Cosmochim Acta 53:399–408. https://doi.org/10.1016/0016-7037(89)90391-8
Buffle J, Wilkinson KJ, Stoll S, Filella M, Zhang J (1998) A generalized description of aquatic colloidal interactions: the three-colloidal component approach. Environ Sci Technol 32:2887–2899. https://doi.org/10.1021/es980217h
Busigny V, Jézéquel D, Cosmidis J, Viollier E, Benzerara K, Planavsky NJ, Albéric P, Lebeau O, Sarazin G, Michard G (2016) The iron wheel in Lac Pavin: Interaction with phosphorus cycle. In: Sime-Ngando T, Boivin P, Chapron E, Jezequel D, Meybeck M (eds) Lake Pavin. Springer, Cham, pp 205–220. https://doi.org/10.1007/978-3-319-39961-4_12
Carrias J-F, Amblard C, Sime-Ngando T (2016) The significance of transparent exopolymeric particles (TEP) for microorganisms in Lake Pavin. In: Sime-Ngando T, Boivin P, Chapron E, Jezequel D, Meybeck M (eds) Lake Pavin. Springer, Cham, pp 223–228. https://doi.org/10.1007/978-3-319-39961-4_13
Chassiot L, Miras Y, Chapron E, Develle A-L, Arnaud F et al (2018) A 7000-year environmental history and soil erosion record inferred from the deep sediments of Lake Pavin (Massif Central, France). Palaeogeogr Palaeoclimatol Palaeoecol 497:218–233. https://doi.org/10.1016/j.palaeo.2018.02.024
Chassiot L, Chapron E, Miras Y, Schwab MJ, Albéric P, Beauger A, Develle AL, Arnaud F, Lajeunesse P, Zocatelli R, et al (2016) Lake Pavin paleolimnology and event stratigraphy. In: Sime-Ngando T, Boivin P, Chapron E, Jezequel D, Meybeck M (eds) Lake Pavin. Springer, Cham, pp 381–406. https://doi.org/10.1007/978-3-319-39961-4_23
Chin W-C, Orellana MV, Verdugo P (1998) Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 391:568–572. https://doi.org/10.1038/35345
Cosmidis J, Benzerara K, Morin G, Busigny V, Lebeau O, Jézéquel D, Noël V, Dublet G, Othmane G (2014) Biomineralization of iron-phosphates in the water column of Lake Pavin (Massif Central, France). Geochim Cosmochim Acta 126:78–96. https://doi.org/10.1016/j.gca.2013.10.037
Défarge C, Trichet J, Maurin A, Hucher M (1994) Kopara in Polynesian atolls: early stages of formation of calcareous stromatolites. Sediment Geol 89:9–23. https://doi.org/10.1016/0037-0738(94)90080-9
Défarge C (1997) Cryoscanning electron microscopy and high resolution scanning electron microscopy of organic matter and organomineral associations in modern microbial sediments. C R Acad Sci Paris Sér Iia 324:553–561 (In French with abridged English version)
Défarge C, Malam Issa O, Trichet J (1999) Field emission cryo-scanning electron microscopy of organic matter and organomineral associations. Application to microbiotic soil crusts. C R Acad Sci Paris, Sciences de la Terre et des planètes 328:591–597. https://doi.org/10.1016/s1251-8050(99)80155-4. (In French with abridged English version)
Du Y, Ramirez C, Jaffé R (2018) Fractionation of DOM by coprecipitation with Fe: effects of composition. Environ Process 5:5–21. https://doi.org/10.1007/s40710-017-0281-4
Hernández R, Sacristán J, Mijangos C (2010) Sol/gel transition of aqueous alginate solutions induced by Fe2+ cations. Macromol Chem Phys 211:1254–1260. https://doi.org/10.1002/macp.200900691
Hu X, Li J, Wang J, Yin L, Shi K, Huang H, Zhang Y, Li S (2023) Characterization and stability of sedimentary colloids in different ecology regions in Taihu Lake. J Oceanol Limnol 41:2146–2159. https://doi.org/10.1007/s00343-022-2254-3
Jaffe AL, Bardot C, Le Jeune A-H, Liu J, Colombet J, Perrière F, Billard H, Castelle CJ, Lehours A-C, Banfield JF (2023) Variable impact of geochemical gradients on the functional potential of bacteria, archaea, and phages from the permanently stratified Lac Pavin. Microbiome 11:14. https://doi.org/10.1186/s40168-022-01416-7
Jézéquel D, Michard G, Viollier E, Agrinier P, Albéric P, Lopes F, Abril G, Bergonzini L (2016) Carbon Cycle in a Meromictic Crater Lake: Lake Pavin, France. In: Sime-Ngando T, Boivin P, Chapron E, Jezequel D, Meybeck M (eds) Lake Pavin. Springer, Cham, pp 185–203. https://doi.org/10.1007/978-3-319-39961-4_11
Jin Q, Zhang L, Liu M (2013) Solvent-polarity-tuned morphology and inversion of supramolecular chirality in a self-assembled pyridylpyrazole-linked glutamide derivative: nanofibers, nanotwists, nanotubes, and microtubes. Chem Eur J 19:9234–9241. https://doi.org/10.1002/chem.201300612
Kerner M, Hohenberg H, Ertl S, Reckermann M, Spitzy A (2003) Self-organization of dissolved organic matter to micelle-like microparticles in river water. Nature 422:150–154. https://doi.org/10.1038/nature01469
Kovač N, Mozetič P, Trichet J, Défarge C (2005) Phytoplankton composition and organic matter organisation of mucous aggregates by means of light and cryo-scanning electron microscopy. Mar Biol 147:261–271. https://doi.org/10.1007/s00227-004-1531-3
Leppard GG (1995) The characterization of algal and microbial mucilages and their aggregates in aquatic ecosystems. Sci Total Environ 165:103–131. https://doi.org/10.1016/0048-9697(95)04546-d
Leppard GG, Massalski A, Lean DSR (1977) Electron-opaque microscopic fibrils in lakes: their demonstration, their biological derivation and their potential significance in the redistribution of cations. Protoplasma 92:289–309. https://doi.org/10.1007/bf01279466
Leppard GG, De Vitre RR, Perret D, Buffle J (1989) Colloidal iron oxyhydroxy-phosphate: the sizing and morphology of an amorphous species in relation to partitioning phenomena. Sci Total Environ 87–88:345–354. https://doi.org/10.1016/0048-9697(89)90247-7
Leppard GG, Burnison BK, Buffle J (1990) Transmission electron microscopy of the natural organic matter of surface waters. Anal Chim Acta 232:107–121. https://doi.org/10.1016/s0003-2670(00)81227-1
Li Q, Cooper RE, Wegner C-E, Taubert M, Jehmlich N, von Bergen M, Küsel K (2021) Insight into autotrophic activities and carbon flow in iron-rich pelagic aggregates (iron snow). Microorganisms 9:1368. https://doi.org/10.3390/microorganisms9071368
Martinez-Pérez AM, Alvarez-Salgado XA, Aristegui J, Nieto-Cid M (2017) Deap-ocean dissolved organic matter reactivity along the Mediterraean Sea: does size matter? Sci Rep 7:5687. https://doi.org/10.1038/s41598-017-05941-6
Michard G, Viollier E, Jézéquel D, Sarazin G (1994) Geochemical study of a crater lake: Pavin Lake, France - Identification, location and quantification of the chemical reactions in the lake. Chem Geol 115:103–115. https://doi.org/10.1016/0009-2541(94)90147-3
Miller MP, McKnight DM, Chapra SC, Williams MW (2009) A model of degradation and production of three pools of dissolved organic matter in an alpine lake. Limnol Oceanogr 54:2213–2227. https://doi.org/10.4319/lo.2009.54.6.2213
Minor EC, Oyler AR (2023) Dissolved organic matter in large lakes: a key but understudied component of the carbon cycle. Biogeochemitry 164:295–318. https://doi.org/10.1007/s10533-020-00733-z
Miot J, Jézéquel D, Benzerara K, Cordier L, Rivas-Lamelo S, Skouri-Panet F, Férard C, Poinsot M, Duprat E (2016) Mineralogical diversity in Lake Pavin: connections with water column chemistry and biomineralization processes. Minerals 6:24. https://doi.org/10.3390/min6020024
Peter S, Isidorova A, Sobek S (2016) Enhanced carbon loss from anoxic lake sediment through diffusion of dissolved organic carbon. J Geophys Res Biogeosci 121:1959–1977. https://doi.org/10.1002/2016jg003425
Reinhardt A (2004) Contrasting roles of natural organic matter on colloidal stabilization and flocculation in freshwaters. Diss Univ Genève. https://doi.org/10.13097/archive-ouverte/unige:275
Rivas-Lamelo S, Benzerara K, Lefèvre C, Monteil C, Jézéquel D, Menguy N et al (2017) Magnetotactic bacteria as a new model for P sequestration in the ferruginous Lake Pavin. Geochem Perspect Lett 5:35–41. https://doi.org/10.7185/geochemlet.1743
Santschi PH, Balnois E, Wilkinson KJ, Zhang J, Buffle J, Guo L (1998) Fibrillar polysaccharides in marine macromolecular organic matter as imaged by atomic force microscopy and transmission electron microscopy. Limnol Oceanogr 43:896–908. https://doi.org/10.4319/lo.1998.43.5.0896
Stoderegger KE, Herndl GH (1999) Production of exopolymer particles by marine bacterioplankton under contrasting turbulence conditions. Mar Ecol Prog Ser 189:9–16. https://doi.org/10.3354/meps189009
Thiam A, Jézéquel D, Groleau A, Prévot F, Lopes F, Albéric P, Quiblier C, Bura-Nakic E, Ciglenecki I, Lazar H, Viollier E (2014) Biogeochemical dynamics of molybdenum in a crater lake: seasonal impact and long-term removal. J Water Resour Prot 6:256–271. https://doi.org/10.4236/jwarp.2014.64031
Thompson DW (1992) On growth and form. Cambridge University Press, Cambridge. https://doi.org/10.2307/3619729
Van Cappellen P, Hyacinthe C (2004) An authigenic iron phosphate phase in estuarine sediments: composition, formation and chemical reactivity. Mar Chem 91:227–251. https://doi.org/10.1016/j.marchem.2004.04.006
Verdugo P (2021) Marine biopolymer dynamics, gel formation, and carbon cycling in the ocean. Gels 7:136. https://doi.org/10.3390/gels7030136
Verdugo P, Santschi PH (2010) Polymer dynamics of DOC networks and gel formation in seawater. Deep-Sea Res 57:1486–1493. https://doi.org/10.1016/j.dsr2.2010.03.002
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. https://doi.org/10.1016/j.marchem.2004.06.017
Vilgé-Ritter A, Rose J, Masion A, Bottero J-Y, Lainé J-M (1999) Chemistry and structure of aggregates formed with Fe-salts and natural organic matter. Colloids Surf A Physicochem Eng Asp 147:297–308. https://doi.org/10.1016/s0927-7757(98)00325-2
Viollier E, Jézéquel D, Michard G, Pèpe M, Sarazin G, Albéric P (1995a) Geochemical study of a crater lake: the Lake Pavin, France - trace element behaviour in the monimolimnion. Chem Geol 125:161–172. https://doi.org/10.1016/0009-2541(95)00059-u
Viollier E, Jézéquel D, Michard G, Pèpe M, Sarazin G (1997) Geochemical study of a crater lake: Lake Pavin, Puy-de-Dôme, France. Constraints afforded by the particulate matter distribution in the element cycling within the lake. Chem Geol 142:225–241. https://doi.org/10.1016/s0009-2541(97)00093-4
Viollier E, Jézéquel D, Michard G, Pèpe M, Sarazin G, Albéric P (1995b) Trace element geochemistry of the Pavin crater lake (France): Chemical reactions and recycling in the monimolimnion. In: Kharaka YK, Chudaev OV (eds) Proceedings of the 8th international symposium of water-rock interaction. AA Balkema, Rotterdam, pp 331–334. https://doi.org/10.1201/9780203734049-82
Wang X, Duan P, Liu M (2013) Organogelation-controlled topochemical [2+2] cycloaddition and morphological changes: from nanofiber to peculiar coaxial hollow toruloid-like nanostructures. Chem Eur J 19:16072–16079. https://doi.org/10.1002/chem.201302200
Wells ML (2002) Marine colloids and trace metals. In : Hansell DA, Carlson CA (eds) Biogeochemistry of Marine Dissolved organic matter. Academic Press, London, pp 367–404. https://doi.org/10.1016/b978-012323841-2/50009-9
Wilkinson KJ, Balnois E, Leppard GG, Buffle J (1999) Characteristic features of the major components of freshwater colloidal organic matter revealed by transmission electron microscopy and atomic force microscopy. Colloids Surf A Physicochem Eng Asp 155:287–310. https://doi.org/10.1016/s0927-7757(98)00874-7
Wilkinson KJ, Reinhardt A (2005) Contrasting roles of natural organic matter on colloidal stabilization and flocculation in freshwaters. In: Droppo IG, Leppard GG, Liss SN, Milligan TG (eds) Flocculation in natural and engineered environmental systems. CRC Press, Boca Raton, pp 143–170. https://doi.org/10.1201/9780203485330.ch7
Zadereev ES, Boehrer B, Gulati RD (2017) Meromictic Lakes, Their Terminology and Geographic Distribution. In: Gulati R, Zadereev E, Degermendzhi A (eds) Ecology of Meromictic Lakes, Ecological Studies 228. Springer, Cham, pp 1–11. https://doi.org/10.1007/978-3-319-49143-1_1
Zark M, Dittmar T (2018) Universal molecular structures in natural dissolved organic matter. Nat Commun 9:3178. https://doi.org/10.1038/s41467-018-05665-9
Zhang L, Wang X, Wang T, Liu M (2015) Tuning soft nanostructures in self-assembled supramolecular gels: from morphology control to morphology-dependent functions. Small 11:1025–1038. https://doi.org/10.1002/smll.201402075
Zhang J, Mostafa KMG et al (2023) Isolation of dissolved organic matter from aqueous solution by precipitation with FeCl3: mechanisms and significance in environmental perspectives. Sci Rep 13:4531. https://doi.org/10.1038/s41598-023-31831-1
Zigah PK, Minor EC, Abdulla HA, Werne JP, Hatcher PG (2014) An investigation of size-fractionated organic matter from Lake Superior and a tributary stream using radiocarbon, stable isotopes and NMR. Geochim Cosmochim Acta 127:264–284. https://doi.org/10.1016/j.gca.2013.11.037
Zigah PK, Minor EC, McNichol AP, Xu L, Werne JP (2017) Constraining the sources and cycling of dissolved organic carbon in a large oligotrophic lake using radiocarbon analyses. Geochim Cosmochim Acta 208:102–118. https://doi.org/10.1016/j.gca.2017.03.021
Acknowledgements
All members of the teams involved in the Metanox and Methanolac projects, and in particular Didier Jézéquel, are thanked for their commitment to the organization of the sampling campaigns and their help during the field work. The municipal authority of Besse-et-Saint-Anastaise is thanked for the provision of facilities on the banks of the lake and Clermont-Auvergne University (formerly Blaise Pascal University) for accommodation at the biological station of Besse-en-Chandesse. François and Hélène Joubert, former hoteliers-restaurateurs of the Lac Pavin Hôtel Restaurant, are kindly thanked for their warm and unfailing welcome. Annie Richard (Centre de Microscopie Electronique of the University of Orléans) helped in Cryo-HRSEM observations and analyses. Elizabeth Rowley-Jolivet helped improve the English. The reviewers are acknowledged for their critical and highly constructive comments.
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Funding was provided through Agence National de la Recherche (ANR) and EC2CO Institut National des Sciences de l'Univers (INSU) under the grants Metanox and Methanolac.
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The planning of the study, sampling and fractionations in the field and geochemical analysis were performed by Patrick Albéric. Supervising cryo-HRSEM observations and analysis were performed by Christian Défarge with Patrick Albéric and the help of the technician of the Centre de Microscopie Electronique of the University of Orléans. The manuscript was drafted by Patrick Albéric, with contributions from Christian Défarge.
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Albéric, P., Défarge, C. Forms of Spontaneous Coagulation and Recycling of Dissolved Organic Carbon in a Monimolimnetic Water Body. Environ. Process. 11, 25 (2024). https://doi.org/10.1007/s40710-024-00699-2
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DOI: https://doi.org/10.1007/s40710-024-00699-2