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Cyanobacterial Contribution to Travertine Deposition in the Hoyoux River System, Belgium

  • Microbiology of Aquatic Systems
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Abstract

Travertine deposition is a landscape-forming process, usually building a series of calcareous barriers differentiating the river flow into a series of cascades and ponds. The process of carbonate precipitation is a complex relationship between biogenic and abiotic causative agents, involving adapted microbial assemblages but also requiring high levels of carbonate saturation, spontaneous degassing of carbon dioxide and slightly alkaline pH. We have analysed calcareous crusts and water chemistry from four sampling sites along the Hoyoux River and its Triffoy tributary (Belgium) in winter, spring, summer and autumn 2014. Different surface textures of travertine deposits correlated with particular microenvironments and were influenced by the local water flow. In all microenvironments, we have identified the cyanobacterium Phormidium incrustatum (Nägeli) Gomont as the organism primarily responsible for carbonate precipitation and travertine fabric by combining morphological analysis with molecular sequencing (16S rRNA gene and ITS, the Internal Transcribed Spacer fragments), targeting both field populations and cultures to exclude opportunistic microorganisms responding favourably to culture conditions. Several closely related cyanobacterial strains were cultured; however, only one proved identical with the sequences obtained from the field population by direct PCR. This strain was the dominant primary producer in the calcareous deposits under study and in similar streams in Europe. The dominance of one organism that had a demonstrated association with carbonate precipitation presented a valuable opportunity to study its function in construction, preservation and fossilisation potential of ambient temperature travertine deposits. These relationships were examined using scanning electron microscopy and Raman microspectroscopy.

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References

  1. Castenholz RW, Rippka R, Herdman M, Wilmotte A (2001) Subsection III. (Formerly Oscillatoriales Elenkin 1934). In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp. 539–562

    Google Scholar 

  2. Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc. Natl. Acad. Sci. 110:1791–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hofmann HJ (1976) Precambrian microflora, Belcher Islands, Canada: significance and systematics. J Palaeontol 50:1040–1073

    Google Scholar 

  4. Golubic S, Hoffmann HJ (1976) Comparison of modern and mid-Precambrian Entophysalidaceae (Cyanophyta) in stromatolitic algal mats: cell division and degradation. J Palaeontol 50:1074–1082

    Google Scholar 

  5. Knoll AH, Golubic S (1992) Proterozoic and living cyanobacteria. In: Schidlowski A (ed) Early organic evolution: implications for mineral and energy resources. Springer, Berlin, pp. 450–462

    Chapter  Google Scholar 

  6. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T (2006) The evolutionary diversification of cyanobacteria: molecular–phylogenetic and paleontological perspectives. P Natl Acad Sci USA 103:5442–5447

    Article  CAS  Google Scholar 

  7. Butterfield NJ (2015) Proterozoic photosynthesis, a critical review. Palaeontology 58:953–972

    Article  Google Scholar 

  8. Walter MR (1976) Stromatolites, Developments in Sedimentology 20. Elsevier, Amsterdam pp. 790

  9. Riding R (1991) Classification of microbial carbonates. In: Riding R (ed) Calcareous algae and stromatolites. Springer, Berlin, pp. 21–51

    Chapter  Google Scholar 

  10. Tewari V, Seckbach J (2011) Stromatolites: interaction of microbes with sediments. Series: Cellular Origin, Life in Extreme Habitats and Astrobiology 18. Springer, Berlin, p. 751

    Google Scholar 

  11. Vincent WF (2000) Cyanobacterial dominance in the polar regions. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Springer, Dordrecht, pp. 321–340

    Google Scholar 

  12. Javaux EJ (2006) Extreme life on past and present Earth, and possibly beyond. Res. Microbiol. 157:37–48

    Article  PubMed  Google Scholar 

  13. Brandes M, Albach DC, Vogt JC, Mayland-Quellhors E, Mendieta-Leiva G, Golubic S, Palinska KA (2015) Supratidal extremophiles—cyanobacterial diversity in the rock pools of the Croatian Adria. Microb. Ecol. 70(4):876–888

    Article  PubMed  Google Scholar 

  14. Pentecost A (1995) The Quaternary travertine deposits of Europe and Asia Minor. Quaternary Sci Rev 14:1005–1028

    Article  Google Scholar 

  15. Ford TD, Pedley HM (1996) A review of tufa and travertine deposits of the world. Earth-Sci. Rev. 41:117–175

    Article  CAS  Google Scholar 

  16. Liu Z, Li Q, Sun H, Liao C, Li H, Wang J, Wu K (2006) Diurnal variations of hydrochemistry in a travertine-depositing stream at Baishuitai, Yunnan, SW China. Aquat. Geochem. 12:103–121

    Article  CAS  Google Scholar 

  17. Arp G, Bissett A, Brinkmann N, Cousin S, De Beer D, Friedl T, Mohr KI, Neu TR, Reimer A, Shiraishi F, Stackebrandt E, Zippel B (2010) Tufa-forming biofilms of German karstwater streams: microorganisms, exopolymers, hydrochemistry and calcification. Geol. Soc. Lond., Spec. Publ. 336:83–118

    Article  CAS  Google Scholar 

  18. Golubic S (1969) Cyclic and noncyclic mechanisms in the formation of travertine. Verhandlungen des Internationalen Verein Limnologie 1:956–961

    Google Scholar 

  19. Golubic S (1964) Beitrag zur Kenntnis der Lichtverhaeltnisse in einigen oligotrophen Seen des Karstes (Light conditions in some oligotrophic lakes of the Karstic region). Carsus Jugoslavicus 4:27–46

    Google Scholar 

  20. Golubic S, Violante C, Plenković A, Grgasović T (2008) Travertines and calcareous tufa deposits: an insight into diagenesis. Geologia Croatica 61:363–378

    Google Scholar 

  21. Pedley HM (2000) Ambient temperature freshwater microbial tufas. In: Riding RE, Awramik SM (eds) Microbial sediments. Springer, Berlin, pp. 179–186

    Chapter  Google Scholar 

  22. Burne RV, Moore LS (1987) Microbialites: organosedimentary deposits of benthic microbial communities. PALAIOS 2:241–254

    Article  Google Scholar 

  23. Pentecost A (2005) Travertine. Springer, Berlin, Heidelberg, New York, p. 448

    Google Scholar 

  24. Allen D, Suchy M (2001) Geochemical evolution of groundwater on Saturna Island, British Columbia. Can J Earth Sci 38:1059–1080

    Article  CAS  Google Scholar 

  25. Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, de Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbio Rev 33:917–941

    Article  CAS  Google Scholar 

  26. De los Ríos A, Ascaso C, Wierzchos J, Fernandez-Valiente E, Quesada A (2004) Microstructural characterization of cyanobacterial mats from the McMurdo Ice Shelf, Antarctica. Appl Environ Microb 70:569–580

    Article  Google Scholar 

  27. Kamennaya N, Ajo-Franklin C, Northen T, Jansson C (2012) Cyanobacteria as biocatalysts for carbonate mineralization. Minerals 2(4):338–364

    Article  CAS  Google Scholar 

  28. Dupraz C, Reid R, Braissant O, Decho AW, Norman RS, Visscher P (2009) Processes of carbonate precipitation in modern microbial mats. Earth-Sci. Rev. 96:141–162

    Article  CAS  Google Scholar 

  29. Chan C (2004) Microbial polysaccharides template assembly of nanocrystal fibers. Science 303:1656–1658

    Article  CAS  PubMed  Google Scholar 

  30. Shiraishi F, Reimer A, Bissett A, de Beer D, Arp G (2008) Microbial effects on biofilm calcification, ambient water chemistry and stable isotope records in a highly supersaturated setting (Westerhöfer Bach, Germany). Palaeogeogr Palaeocl 262:91–106

    Article  Google Scholar 

  31. Bartley JK (1996) Actualistic taphonomy of Cyanobacteria: implications for the Precambrian fossil record. PALAIOS 11:571–586

    Article  Google Scholar 

  32. Golubic S, Fischer AG (1975) Ecology of calcareous nodules forming in Little Connestoga Creek near Lancaster, Pennsylvania. Verhandlungen des Internationalen Verein Limnologie 19:2315–2323

    Google Scholar 

  33. Golubic S, Violante C, Ferreri V, D’Argenio B (1993) Algal control and early diagenesis in Quaternary travertine formation (Rocchetta a Volturno, Central Apennines). In Barattolo F, De Castro P, Parente M (eds) Studies on fossil benthic algae. Bollettino Società Paleontologica Italiana, Special Volume 1: pp. 231–247.

  34. Lepot K, Deremiens L, Namsaraev Z, Compère P, Gérard E, Verleyen E, Tavernier I, Hodgson DA, Wilmotte A, Javaux EJ (2014) Organo-mineral imprints in fossil cyanobacterial mats of an Antarctic lake. Geobiology 12(5):424–450

    Article  CAS  PubMed  Google Scholar 

  35. Cousin S, Stackebrandt E (2010) Spatial bacterial diversity in a recent freshwater tufa deposit. Geomicrobiology J 27:275–291

    Article  CAS  Google Scholar 

  36. Brinkmann N, Hodac L, Mohr KI, Hodacova A, Jahn R, Ramm J, Hallmann C, Arp G, Friedl T (2015) Cyanobacteria and diatoms in biofilms of two karstic streams in Germany and changes of their communities along calcite saturation gradients. Geomicrobiology J 32:255–274

    Article  CAS  Google Scholar 

  37. Franco B, Houbrechts G, Van Campehout JE, Hallot E, Petit F (2008) Etude géomorphologique des barrages de travertin du Hoyoux. Bulletin de la Société géographique de Liège 50:45–56

    Google Scholar 

  38. Borges AV, Darchambeau F, Teodoru CR, Marwick TR, Tamooh F, Geeraert N, Omengo FO, Guérin F, Lambert T, Morana C, Okuku E, Bouillon S (2015) Globally significant greenhouse gas emissions from African inland waters. Nat. Geosci. 8:637–642

    Article  CAS  Google Scholar 

  39. Abril G, Bouillon S, Darchambeau F, Teodoru CR, Marwick TR, Tamooh F, Omengo FO, Geeraert N, Deirmendjian L, Polsenaere P, Borges AV (2015) Technical Note: Large overestimation of pCO2 calculated from pH and alkalinity in acidic, organic-rich freshwaters. Biogeosciences 12(1):67–78

    Article  CAS  Google Scholar 

  40. Gran G (1952) Determination of the equivalence point in potentiometric titrations of seawater with hydrochloric acid. Oceanol. Acta 5:209–218

    Google Scholar 

  41. Rodier J, Bazin C, Broutin JP, Chambon P, Champsaur H, Rodi L (2005) L'analyse de l'eau: eaux naturelles, eaux résiduaires, eau de mer. Paris. 8th edn, pp. 1381

  42. Marshall CP, Javaux EJ, Knoll AH, Walter MR (2005) Combined micro-Fourier transform infrared (FTIR) spectroscopy and micro-Raman spectroscopy of Proterozoic acritarchs: a new approach to palaeobiology. Precambrian Res. 138(3–4):208–224

    Article  CAS  Google Scholar 

  43. Storme JY, Golubic S, Wilmotte A, Kleinteich J, Velázquez D, Javaux EJ (2015) Raman characterization of the UV-protective pigment gloeocapsin and its role in the survival of cyanobacteria. Astrobiology 15:843–857

    Article  CAS  PubMed  Google Scholar 

  44. Stanier RY, Kunisawa R, Mandel M, Cohenbazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35:171–205

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Jungblut AD, Neilan BA (2006) Molecular identification and evolution of the cyclic peptide hepatotoxins, microcystin and nodularin, synthetase genes in three orders of cyanobacteria. Arch. Microbiol. 185:107–114

    Article  CAS  PubMed  Google Scholar 

  46. Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microb 63:3327–3332

    Google Scholar 

  47. Taton A, Grubisic S, Brambilla E, Wit D, Wilmotte A (2003) Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl Environ Microb 69:5157–5169

    Article  CAS  Google Scholar 

  48. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp 41:95–98

    CAS  Google Scholar 

  49. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Van de Peer Y, De Wachter R (1997) Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J. Mol. Evol. 45:619–630

    Article  CAS  PubMed  Google Scholar 

  51. Jukes TH and Cantor CR (1969) Evolution of protein molecules. In Munro HN (ed.) Mammalian protein metabolism. Academic Press, New York and London. Volume III Chapter 24

  52. Grossman AR (2003) A molecular understanding of complementary chromatic adaptation. Photosynth. Res. 76:207–215

    Article  CAS  PubMed  Google Scholar 

  53. Tandeau de Marsac N (1977) Occurrence and nature of chromatic adaptation in cyanobacteria. J. Bacteriol. 130:82–91

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Pentecost A (2003) Taxonomic identity, ecology and distribution of the calcite-depositing cyanobacterium Phormidium incrustatum (Oscillatoriaceae). Cryptogamie Algol 24:307–321

    Google Scholar 

  55. Bartrons M, Catalan J, Casamayor EO (2012) High bacterial diversity in epilithic biofilms of oligotrophic mountain lakes. Microb. Ecol. 64:860–869

    Article  PubMed  Google Scholar 

  56. Hašler P, Dvořak P, Johansen JR, Kitner M, Ondřej V, Pouličkova A (2012) Morphological and molecular study of epipelic filamentous genera Phormidium, Microcoleus and Geitlerinema (Oscillatoriales, Cyanophyta/Cyanobacteria). Fottea 12(2):341–356

    Google Scholar 

  57. Golubic S (1973) The relationship between blue-green algae and carbonate deposits. In: Carr N, Whitton BA (eds) The biology of blue-green algae. Blackwell, Oxford, pp. 434–472

    Google Scholar 

  58. Herman SH, Lorah MM (1987) CO2 outgassing and calcite precipitation in falling spring creek, Virginia, USA. Chem. Geol. 62:251–262

    Article  CAS  Google Scholar 

  59. Suda S, Watanabe MM, Otsuka S, Mahakahant A, Yongmanitchai W, Nopartnaraporn N, Liu Y, Day JG (2002) Taxonomic revision of water bloom–forming species of oscillatorioid cyanobacteria. Int J Syst Evol Micr 52:1577–1595

    CAS  Google Scholar 

  60. Schneider D, Reimer A, Hahlbrock A, Arp G, Daniel R (2015) Metagenomic and metatranscriptomic analyses of bacterial communities derived from a calcifying karst water creek biofilm and tufa. Geomicrobiol J. 32:316–331

    Article  CAS  Google Scholar 

  61. Palińska KA, Abed RMM, Wendt K, Charpy L, Łotocka M, Golubic S (2012) Opportunistic cyanobacteria in benthic microbial mats of a tropical lagoon, Tikehau Atoll, Tuamotu Archipelago: minor in natural populations, major in cultures. Fottea 12:127–140

    Article  Google Scholar 

  62. Richert L, Golubic S, De Le Gue R, Herve A, Payri C (2006) Cyanobacterial populations that build ‘kopara’ microbial mats in Rangiroa, Tuamotu Archipelago, French Polynesia. Europ J Phycol 41:259–279

    Article  CAS  Google Scholar 

  63. Engene N, Hyukjae Choi EC, Ellisman MH, Komárek J, Gerwick WH (2012) Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int J Syst Evol Micr 62:1171–1178

    Article  Google Scholar 

  64. Komárek J, Kaštovský J, Mareš J, Johansen JR (2014) Taxonomic classification of cyanoprokaryotes (cyanobacterial genera), using a polyphasic approach. Preslia 86:295–335

    Google Scholar 

  65. Merz-Preiss M (2000) Calcification in Cyanobacteria. In: Riding RE, Awramik SM (eds) Microbial sediments. Springer, Berlin, pp. 50–56

    Chapter  Google Scholar 

  66. Srdoč D, Horvatinčić N, Obelić B, Krajcar-Bronić I, Sliepčević A (1985) Calcite deposition processes in karstwaters with special emphasis on the Plitvice Lakes, Yugoslavia (Croatian w. German and English summary). Krš Jugoslavije (Carsus Iugoslaviae) 11:101–204

    Google Scholar 

  67. Berrendero E, Arenas C, Mateo P, Jones B (2016) Cyanobacterial diversity and related sedimentary facies as a function of water flow conditions: example from the Monasterio de Piedra Natural Park (Spain). Sed Geol 337:12–28

    Article  CAS  Google Scholar 

  68. Golubic S, Lee S-J, Browne KM (2000) Cyanobacteria: architects of sedimentary structures. In: Riding RE, Awramik (eds) Microbial sediments. Springer, Heidelberg-Berlin-New York, pp. 56–67

    Google Scholar 

  69. Le Campion-Alsumard T, Golubic S, Hutchings P (1995) Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar Ecol-Prog Ser 117:149–157

    Article  Google Scholar 

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Acknowledgements

We acknowledge the Marie Curie COFUND-BeIPD for fellowship to J.K., the FRS-FNRS (Fonds De La Recherche Scientifique) grant to S.G. for sabbatical stay in A.W. and E.J.J.’s laboratories, the FNRS credit CR.CH.10-11-1.5139.11 and FRFC 2.4570.09, the FP7 ERC Stg ELiTE and the Belspo IAP PLANET TOPERS to E.J.J. and ERC postdoc to J.-Y.S. Collaborative field research support to S.G. and S.J.L. was provided by the National R&D Project hosted by the National Research Institute of Cultural Heritage in Cultural Heritage Administration, Korea. International collaboration was supported by Alexander-von Humboldt Foundation, Bonn and Hanse Institute for Advanced Studies, Delmenhorst to S.G. We are grateful to E. Poty for guidance in the field and A. Beulen and S. Petrovic for assistance in field sampling and laboratory analysis. The authors thank the Centre of Aid for Research and Education in Microscopy of the University of Liege (CAREM-ULg) for providing access to performant equipment in electron microscopy. The water discharge data was freely provided by Service public de Wallonie, Direction générale opérationnelle Mobilité et Voies hydrauliques, Direction de la Gestion hydrologique intégrée, Service d’Etudes Hydrologiques (SETHY). A.V.B. is senior research associate and A.W. is research associate of the FRS-FNRS.

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Authors and Affiliations

  1. InBios Center for Protein Engineering, University of Liège, B-4000, Liège, Belgium

    Julia Kleinteich, Stjepko Golubic, Igor S. Pessi, David Velázquez & Annick Wilmotte

  2. Center for Applied Geosciences, University of Tübingen, D-72074, Tübingen, Germany

    Julia Kleinteich

  3. Biological Science Center, Boston University, Boston, MA, 02215, USA

    Stjepko Golubic

  4. Palaeobiogeology, Palaeobotany, Palaeopalynology, Department of Geology, UR Geology B18, University of Liège, B-4000, Liège, Belgium

    Stjepko Golubic, Jean-Yves Storme & Emmanuelle J. Javaux

  5. Department of Biology, Universidad Autónoma de Madrid, E-28049, Madrid, Spain

    David Velázquez

  6. Chemical Oceanography Unit, Institut de Physique (B5), University of Liege, B-4000, Liège, Belgium

    François Darchambeau & Alberto V. Borges

  7. Department of Biology, Ecology and Evolution (BEE)/Centre of Aid for Research and Education in Microscopy (CAREM), University of Liège, B-4000, Liège, Belgium

    Philippe Compère

  8. Hessisches Landesamt für Naturschutz, Umwelt und Geologie, Rheingaustr. 186, D-65203, Wiesbaden, Germany

    Gudrun Radtke

  9. Department of Geology, Kyungpook National University, 1370 Sankyuck-dong, Daegu, 702-701, South Korea

    Seong-Joo Lee

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  1. Julia Kleinteich
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Correspondence to Julia Kleinteich.

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Kleinteich, J., Golubic, S., Pessi, I.S. et al. Cyanobacterial Contribution to Travertine Deposition in the Hoyoux River System, Belgium. Microb Ecol 74, 33–53 (2017). https://doi.org/10.1007/s00248-017-0937-7

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