Specific carbonate-microbe interactions in the modern microbialites of Lake Alchichica (Mexico)

ISME Journal

Volumn 7, Issue 10, 2013, Pages 1997-2009

  Gérard, Emmanuelle ^a   Ménez, Bénédicte ^a   Couradeau, Estelle ^a,b,c   Moreira, David ^c   Benzerara, Karim ^b   Tavera, Rosaluz ^d   López García, Purificación ^c  

^a INSTITUT DE PHYSIQUE DU GLOBE DE PARIS   (France)

^b UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^c UNIVERSITÉ PARIS SUD   (France)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Aragonite; Confocal laser scanning microscopy; Hydromagnesite; Microbialites; Pleurocapsales; Raman spectroscopy

Indexed keywords

CARBONIC ACID DERIVATIVE; PIGMENT;

ARAGONITE; BIOFILM; CARBONATE; ENVIRONMENTAL CONDITIONS; FLUORESCENCE; FOSSIL; MICROBIAL ECOLOGY; MICROBIALITE; MICROORGANISM; MINERAL; MORPHOLOGY; PRECAMBRIAN; RAMAN SPECTROSCOPY;

ARTICLE; BIOFILM; CHEMISTRY; CLASSIFICATION; CONFOCAL MICROSCOPY; CYANOBACTERIUM; LAKE; METABOLISM; MEXICO; MICROBIOLOGY; PHYLOGENY; RAMAN SPECTROMETRY; ULTRASTRUCTURE;

BIOFILMS; CARBONATES; CYANOBACTERIA; LAKES; MEXICO; MICROSCOPY, CONFOCAL; PHYLOGENY; PIGMENTS, BIOLOGICAL; SPECTRUM ANALYSIS, RAMAN;

LAKE ALCHICHICA; MEXICO [NORTH AMERICA]; PUEBLA [MEXICO];

BACILLARIOPHYTA; CHROOCOCCALES; CYANOBACTERIA; EUKARYOTA; NOSTOCALES; OSCILLATORIALES; PLEUROCAPSA; PLEUROCAPSALES;

EID: 84884675825     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.81     Document Type: Article

References (58)

1. Amann R, Fuchs BM. (2008). Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat Rev 6: 339-348
2. Arp G, Reimer A, Reitner J. (2003). Microbialite formation in seawater of increased alkalinity, Satonda Crater Lake, Indonesia. J Sediment Res 73: 105-127
3. Arp G, Reimer A, Reitner J. (1999). Calcification in cyanobacterial biofilms of alkaline salt lakes. Eur J Phycol 34: 393-403
4. Arp G, Reimer A, Reitner J. (2001). Photosynthesisinduced biofilm calcification and calcium concentrations in Phanerozoic oceans. Science 292: 1701-1704
5. Awramik SM, Sprinkle J. (1999). Proterozoic stromatolites: The first marine evolutionary biota. Hist Biol 13: 241-253
6. Benzerara K, Menguy N, Lopez-Garcia P, Yoon TH, Kaźmierczak J, Tyliszczak T et al. (2006). Nanoscale detection of organic signatures in carbonate microbialites. Proc Natl Acad Sci USA 103: 9440-9445
7. Benzerara K, Menguy N. (2009). Looking for traces of life in minerals. Compt Rend Palevol 8: 617-628
8. Beyssac O, Lazzeri M. (2012). Application of Raman microspectroscopy to the study of graphitic carbon materials in Earth Sciences. In: Dubessy J, Caumon M-C, Ruff F (eds). EMU Notes in Mineralogy- Applications of Raman spectroscopy to Earth sciences and cultural heritage. Mineralogical Society: Twickenham, UK, Chapter 12
9. Braissant O, Cailleu G, Dupraz C, Verrecchia EP. (2003). Bacterially induced mineralization of calcium carbonate in terrestrial environments: The role of exopolysaccharides and amino acids. J Sediment Res 73: 485-490
10. Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher PT. (2007). Exopolymeric substances of sulfate-reducing bacteria: Interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5: 401-411
11. Braissant O, Decho AW, Przekop KM, Gallagher KL, Glunk C, Dupraz C et al. (2009). Characteristics and turnover of exopolymeric substances in a hypersaline microbial mat. FEMS Microbiol Ecol 67: 293-307
12. Buick R, Dunlop JSR, Groves DI. (1981). Stromatolite recognition in ancient rocks: An appraisal of irregularly laminated structures in an Early Archaean chertbarite unit from North Pole, Western Australia. Alcheringa 5: 161-181
13. Büdel B, Rhiel E. (1985). A new cell wall structure in a symbiotic and free-living strain of the blue-green alga genus Chroococcidiopsis (Pleurocapsales). Arch Micrbiol 143: 117-121
14. Couradeau E, Benzerara K, Gérard E, Estève I, Moreira D, Tavera R et al. (2013). Cyanobacterial calcification in modern microbialites at the submicrometer-scale. Biogeosci Discuss 10: 3311-3339
15. Couradeau E, Benzerara K, Gérard E, Moreira D, Bernard S, Brown Jr GE et al. (2012). An early-branching microbialite cyanobacterium forms intracellular carbonates. Science 336: 459-462
16. Couradeau E, Benzerara K, Moreira D, Gérard E, Kazmierczak J, Tavera R et al. (2011). Prokaryotic and eukaryotic community structure in field and cultivated microbialites from the alkaline lake of Alchichica (Mexico). PloS ONE 6: E28767
17. Decho AW, Visscher PT, Reid RP. (2005). Production and cycling of natural microbialexopolymers (EPS) within a marine stromatolite. Palaeogeography, Palaeoclimatology. Palaeoecology 219: 71-86
18. Deleuze M, Brantley SL. (1997). Inhibition of calcite crystal growth by Mg2 at 1001C and 100 bars: Influence of growth regime. Geochim Cosmochim Acta 61: 1475-1485
19. Dill RF, Shinn EA, Jones AT, Kelly K, Steinen RP. (1986). Giant subtidal stromatolites forming in normal salinity waters. Nature 324: 55-58
20. Downs RT. (2006). The RRUFF Project: An integrated study of the chemistry, crystallography, Raman and infrared spectroscopy of minerals. Program and Abstracts of the 19th General Meeting of the International Mineralogical Association in Kobe, Japan O03-13
21. Dravis JJ. (1983). Hardened subtidal stromatolites, Bahamas. Science 219: 385-386
22. Dupraz C, Reid RP, Braissant O, Decho AW, Norman RS, Visscher PT. (2009). Processes of carbonate precipitation in modern microbial mats. Earth Sci Rev 96: 141-152
23. Dupraz C, Visscher PT. (2005). Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol 13: 429-438
24. Foster JS, Green SJ, Ahrendt SR, Golubic S, Reid RP, Hetherington KL et al. (2009). molecular and morphological characterisation of cyanobacterial diversity in the stromatolites of highborne Cay, Bahamas. ISME J 3: 573-587
25. Goh F, Allen MA, Leuko S, Kawaguchi T, Decho AW, Burns BP et al. (2009). Determining the specific microbial populations and their spatial distribution within the stromatolite ecosystem of Shark Bay. ISME J 3: 383-396
26. Grotzinger JP, Knoll AH. (1999). Stromatolites in Precambrian carbonates: Evolutionary mileposts or environmental dipsticks? Annu Rev Earth Planet Sci 27: 313-358
27. Hall EK, Singer GA, Polzl M, Hammerle I, Schwarz C, Daims H et al. (2010). Looking inside the box: Using Raman microspectroscopy to deconstruct microbial biomass stoichiometry one cell at a time. ISME J 5: 196-208
28. Huang WE, Fergusson A, Singer AC, Lawson K, Thompson IP, Kalin RM et al. (2009). Resolving genetic functions within microbial population: In situ analyses using rRNA and mRNA stable isotope probing coupled with single-cell-Raman-fluorescence in situ hybridization. Appl Environ Microbiol 75: 234-241
29. Huang WE, Mengqiu L, Jarvis RM, Goodacre R, Banwart SA. (2010). Shining light on the microbial world: The application of Raman microspectroscopy. Adv Appl Microbiol 70: 153-186
30. Huang WE, Stoecker K, Griffiths R, Newbold L, Daims H, Whiteley AS et al. (2007). Raman-FISH: Combining stable isotope Raman spectroscopy and fluorescence in situ hybridization for single cell analysis of identity and function. Environ Microbiol 9: 1878-1889
31. Kah LC, Knoll AH. (1996). Microbenthic distribution of Proterozoic tidal flats: Environmental and taphonomic considerations. Geology 24: 79-82
32. Kawaguchi T, Decho AW. (2002). In situ microspatial imaging using two-photon and confocal laser scanning microscopy of bacteria and extracellular polymeric secretions (EPS) within marine stromatolites. Marine Biotechnol 4: 127-131
33. Kaźmierczak J, Kempe S, Kremer B, López-García P, Moreira D, Tavera R. (2011). Hydrochemistry and microbialites of the alkaline crater lake Alchichica, Mexico. Facies 57: 543-570
34. Kempe S, Kaźmierczak J, Landmann G, Konuk T, Reimer A, Lipp A. (1991). Largest known microbialites discovered in Lake Van, Turkey. Nature 349: 605-608
35. Kempe S, Kaźmierczak J. (1993). Satonda Crater Lake, Indonesia: Hydrogeochemistry and biocarbonates. Facies 28: 1-31
36. Kempe S, Kaz'mierczak J. (1994). The role of alkalinity in the evolution of ocean chemistry, organization of living systems, and biocalcification processes In: Doumenge F, Allemand D, Toulemont A (eds). Past and Present Biomineralization Processes. Considerations About the Carbonate Cycle. Institut Océanographique: Monaco, pp 61-117
37. Knoll AH, Semikhatov MA. (1998). The genesis and time distribution of two distinctive proterozoic stromatolite microstructures. Palaios 13: 408-422
38. Komárek J, Hauer T. (2011). CyanoDB.cz On-line database of cyanobacterial genera. Univ. of South Bohemia and Inst. of Botany AS CRhttp://www.cyanodb.cz
39. Kremer B, Kaz'mierczak J, Stal LJ. (2008). Calcium carnonate precipitation in cyanobacterial mats from sandy tidal falts of the North Sea. Geobiology 6: 46-56
40. Lepot K, Benzerara K, Brown GEJ, Philippot P. (2008). Microbially influenced formation of 2.724-millionyear- old stromatolites. Nat Geosci 1: 118-121
41. Lepot K, Benzerara K, Brown GEJ, Philippot P. (2009). Organic matter heterogeneity in 2.72 Ga stromatolites: Alteration versus preservation by sulphur incorporation. Geochim Cosmochim Acta 73: 6579-6599
42. Logan BW. (1961). Cryptozoon and associated stromatolites from the recent, Shark Bay, Western Australia. J Geol 69: 517-533
43. López-García P, Kaźmierczak J, Benzerara K, Kempe S, Guyot F, Moreira D. (2005). Bacterial diversity and carbonate precipitation in the giant microbialites from the highly alkaline Lake Van, Turkey. Extremophiles 9: 263-274
44. Ludwig R, Al-Horani FA, de Beer D, Jonkers HM. (2005). Photosynthesis-controlled calcifification in a hypersaline microbial mat. Limnol Oceonogr 50: 1836-1843
45. Moran AL. (2000). Calcein as a marker in experimental studies newly-hatched gastropods. Marine Biol 137: 893-898
46. Obst M, Dynes JJ, Lawrence JR, Swerhone GDW, Benzerara K, Karunakaran C et al. (2009). Precipitation of amorphous CaCO3 (aragonite-like) by cyanobacteria: ASTXM study of the influence of EPS on the nucleation process. Geochim Cosmochim Acta 73: 4180-4198
47. Planavsky N, Reid RP, Lyons TW, Myshrall KL, Visscher PT. (2009). Formation and diagenesis of modern marine calcified cyanobacteria. Geobiology 7: 566-576
48. Reid RP, Browne KM. (1991). Intertidal stromatolites in a fringing Holocene reef complex in the Bahamas. Geology 19: 15-18
49. Reid RP, James NP, Macintyre IG, Dupraz CP, Burne RV. (2003). Shark Bay stromatolites: Microfabrics and reinterpretation of origins. Facies 49: 45-53
50. Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C et al. (2000). The role of microbes in accretion, lamination and early lithification of modern marine stromatolites. Nature 406: 989-992
51. Rividi N, Van Zuilen M, Philippot P, Menez B, Godard G, Poidatz E. (2010). Calibration of carbonate composition using micro-Raman analysis: Application to planetary surface exploration. Astrobiology 10: 293-309
52. Schultze-Lam S, Beveridge TJ. (1994). Nucleation of celestite and strontianite on a cyanobacterial S-layer. Appl Environ Microbiol 60: 447-453
53. Stanley SM, Hardie LA. (1999). Hypercalcification: Paleontology links plate plate tectonics and geochemistry to sedimentology. GSA Today 9: 1-7
54. Wagner M, Ivleva NP, Haisch C, Niessner R, Horn H. (2009). Combined used of confocal laser scanning microscopy (CLSM) and Raman Microscopy (RM): Investigation on EPS-matrix. Water Res 43: 63-76
55. Wagner M. (2009). Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu Rev Microbiol 63: 411-429
56. Waterbury JB, Stanier RY. (1978). Patterns of growth and development in Pleurocapsalean cyanobacteria. Microbiol Rev 42: 2-44
57. Zeebe RE, Wolf-Gladrow DA. (2001). In CO2 in Seawater: Equilibrium, Kinetics, Isotopes. Halpern D (ed. 65 Elsevier Oceanography Series: Amsterdam 346
58. Zippel B, Neu TR. (2011). Characterization of glycoconjugates of extracellular polymeric substances in tufaassociated biofilms by using fluorescence lectin-binding analysis. Appl Environ Microbiol 77: 505-516.