Active bacteria and archaea cells fixing bicarbonate in the dark along the water column of a stratified eutrophic lagoon

FEMS Microbiology Ecology

Volumn 77, Issue 2, 2011, Pages 370-384

  Llirós, Marc ^a   Alonso Sáez, Laura ^b   Gich, Frederic ^a   Plasencia, Anna ^a   Auguet, Olga ^a   Casamayor, Emilio O ^b   Borrego, Carles M ^a  

^a UNIVERSITY OF GIRONA   (Spain)

^b CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

Author keywords

Anaplerotic reactions; Chemoautotrophy; Dark carbon fixation; Heterotrophic carbon fixation; Karstic lakes; Sulfidic redoxclines

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; BICARBONATE; CARBON; CARBON DIOXIDE; FRESH WATER; RNA 16S;

BICARBONATE; CARBON DIOXIDE; CARBON FIXATION; CLONE; COASTAL LAGOON; DARK; DOMINANCE; EPILIMNION; EUTROPHICATION; GENETIC ANALYSIS; HETEROTROPHY; KARST HYDROLOGY; MICROBIAL COMMUNITY; MICROPLANKTON; PROKARYOTE; REDOX CONDITIONS; STRATIFICATION; TRANSITION ZONE; WATER COLUMN;

ARCHAEAL GENE; ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENE; BACTERIUM; CARBON CYCLE; CHEMISTRY; CLASSIFICATION; DARKNESS; DENATURING GRADIENT GEL ELECTROPHORESIS; FLUORESCENCE IN SITU HYBRIDIZATION; GENE LIBRARY; GENETICS; METABOLISM; MICROBIOLOGY; PHYLOGENY;

ACETYL-COA CARBOXYLASE; ARCHAEA; BACTERIA; BICARBONATES; CARBON CYCLE; CARBON DIOXIDE; CARBON ISOTOPES; DARKNESS; DENATURING GRADIENT GEL ELECTROPHORESIS; FRESH WATER; GENE LIBRARY; GENES, ARCHAEAL; GENES, BACTERIAL; IN SITU HYBRIDIZATION, FLUORESCENCE; PHYLOGENY; RNA, RIBOSOMAL, 16S; WATER MICROBIOLOGY;

ARCHAEA; BACTERIA (MICROORGANISMS); BACTEROIDETES; BETAPROTEOBACTERIA; CHLOROBI; CRENARCHAEOTA;

EID: 79960153422     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2011.01117.x     Document Type: Article

References (98)

1. Alonso C & Pernthaler J (2005) Incorporation of glucose under anoxic conditions by bacterioplankton from coastal North Sea surface waters. Appl Environ Microb 71: 1709-1716.
2. Alonso-Saez L, Galand PE, Casamayor EO, Pedros-Alio C & Bertilsson S (2010) High bicarbonate assimilation in the dark by Arctic bacteria. ISME J 4: 1581-1590.
3. Amann R & Fuchs BM (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat Rev Microbiol 6: 339-348.
4. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R & Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microb 56: 1919-1925.
5. Auguet JC, Borrego CM, Baneras L & Casamayor EO (2008) Fingerprinting the genetic diversity of the biotin carboxylase gene (accC) in aquatic ecosystems as a potential marker for studies of carbon dioxide assimilation in the dark. Environ Microbiol 10: 2527-2536.
6. Auguet JC, Barberan A & Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4: 182-190.
7. Battin TJ, Wille A, Sattler B & Psenner R (2001) Phylogenetic and functional heterogeneity of sediment biofilms along environmental gradients in a glacial stream. Appl Environ Microb 67: 799-807.
8. Berg IA, Kockelkorn D, Buckel W & Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318: 1782-1786.
9. 2 fixation cycles in Crenarchaeota. Microbiology 156: 256-269.
10. Biddle JF, Lipp JS, Lever MA et al. (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. P Natl Acad Sci USA 103: 3846-3851.
11. Borrego C & Garcia-Gil J (1994) Caracterización limnológica de la Coromina, una laguna hipereutrófica del sistema lacustre de Banyoles. Limnética 10: 43-51.
12. Borrego CM & Garcia-Gil LJ (1995) Rearrangement of light harvesting bacteriochlorophyll homologs as a response of Green Sulfur Bacteria to low light intensities. Photosynth Res 45: 21-30.
13. Brock TD, Brock ML, Bott TL & Edwards MR (1971) Microbial life at 90°C: the sulfur bacteria of Boulder Spring. J Bacteriol 107: 303-314.
14. Buck U, Grossart HP, Amann R & Pernthaler J (2009) Substrate incorporation patterns of bacterioplankton populations in stratified and mixed waters of a humic lake. Environ Microbiol 11: 1854-1865.
15. Camacho A & Vicente E (1998) Carbon photoassimilation by sharply stratified phototrophic communities at the chemocline of Lake Arcas (Spain). FEMS Microbiol Ecol 25: 11-22.
16. Camacho A, Erez J, Chicote A, Florin M, Squires MM, Lehmann C & Bachofen R (2001) Microbial microstratification, inorganic carbon photoassimilation and dark carbon fixation at the chemocline of the meromictic Lake Cadagno (Switzerland) and its relevance to the food web. Aquat Sci 63: 91.
17. 2 fixation rates in lakes with oxygen-sulfide interfaces. Aquat Microb Ecol 59: 217-228.
18. Casamayor EO & Borrego CM (2009) Archaea. Encyclopedia of Inland Waters, Vol. 3 (Likens GE, ed), pp. 167-181. Elsevier, Oxford.
19. Casamayor EO, Schafer H, Baneras L, Pedros-Alio C & Muyzer G (2000) Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microb 66: 499-508.
20. Casamayor EO, Muyzer G & Pedrós-Alió C (2001) Composition and temporal dynamics of planktonic archaeal assemblages from anaerobic sulfurous environments studied by 16S rDNA denaturing gradient gel electrophoresis and sequencing. Aquat Microb Ecol 25: 237-246.
21. Casamayor EO, García-Cantizano J & Pedrós-Alió C (2008) Carbon dioxide fixation in the dark by photosynthetic bacteria in sulfide-rich stratified lakes with oxic-anoxic interfaces. Limnology and Oceanography. Limnol Oceanogr 53: 1193-1203.
22. Chaban B, Ng SY & Jarrell KF (2006) Archaeal habitats-from the extreme to the ordinary. Can J Microbiol 52: 73-116.
23. Cloern JE, Cole BE & Oremland RS (1983) Autotrophic processes in meromictic Soda Lake, Nevada. Limnol Oceanogr 28: 1049-1061.
24. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M & Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
25. Culver DA & Brunskill GJ (1969) Fayetteville Green Lake, New York. V. Studies of primary production and zooplankton in a meromictic marl lake. Limnol Oceanogr 14: 862-873.
26. Daims H, Brühl A, Amann R, Schleifer K & Wagner M (1999) The domain-specific probe eub338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434-444.
27. De Haan H (1972) Molecular-size distribution of soluble humic compounds from different natural waters. Freshwater Biol 2: 235-241.
28. DeLong EF (1992) Archaea in coastal marine environments. P Natl Acad Sci USA 89: 5685-5689.
29. DeLong EF (1998) Everything in moderation: archaea as 'non-extremophiles'. Curr Opin Genet Dev 8: 649-654.
30. DeLong EF & Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50: 470-478.
31. Dijkhuizen L & Harder W (1984) Current views on the regulation of autotrophic carbon dioxide fixation via the Calvin cycle in bacteria. Anton Leeuw Int J G 50: 473-487.
32. Dijkhuizen L & Harder W (1985) Microbial metabolism of carbon dioxide. Comprehensive Biotechnology, Vol. 1 (Dalton H, ed), pp. 409-423. Pergamon Press, Oxford.
33. Eiler A & Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ Microbiol 6: 1228-1243.
34. Felsenstein J (2007) PHYLIP (Phylogeny Inference Package). Department of Genetics, University of Washington, Seattle, WA.
35. 2 incorporation among planktonic microbial guilds and estimation of in situ specific growth rates. Microb Ecol 50: 230-241.
36. Gasol JM, García-Cantizano J, Massana R, Guerrero R & Pedrós-Alió C (1993) Physiological ecology of a metalimnetic Cryptomonas population: relationships to light, sulfide, and nutrients. J Plankton Res 15: 255-275.
37. Gich FB, Borrego CM, Martínez-Planells A, Steensgaard DB, Garcia-Gil LJ & Holzwarth AR (2001) Variability of the photosynthetic antenna of a Pelodictyon clathratiforme population from a freshwater holomictic pond. FEMS Microbiol Ecol 37: 11-19.
38. Glaubitz S, Lueders T, Abraham WR, Jost G, Jurgens K & Labrenz M (2009) 13C-isotope analyses reveal that chemolithoautotrophic Gamma- and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea. Environ Microbiol 11: 326-337.
39. Glaubitz S, Labrenz M, Jost G & Jurgens K (2010) Diversity of active chemolithoautotrophic prokaryotes in the sulfidic zone of a Black Sea pelagic redoxcline as determined by rRNA-based stable isotope probing. FEMS Microbiol Ecol 74: 32-41.
40. Gomez-Consarnau L, Gonzalez JM, Coll-Llado M et al. (2007) Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445: 210-213.
41. Gonzalez JM, Fernandez-Gomez B, Fernandez-Guerra A et al. (2008) Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). P Natl Acad Sci USA 105: 8724-8729.
42. Grote J, Labrenz M, Pfeiffer B, Jost G & Jurgens K (2007) Quantitative distributions of Epsilonproteobacteria and a Sulfurimonas subgroup in pelagic redoxclines of the central Baltic Sea. Appl Environ Microb 73: 7155-7161.
43. Grote J, Jost G, Labrenz M, Herndl GJ & Jurgens K (2008) Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl Environ Microb 74: 7546-7551.
44. Guerrero R, Montesinos E, Pedrós-Alió C et al. (1985) Phototrophic sulfur bacteria in two Spanish lakes: vertical distribution and limiting factors. Limnol Oceanogr 30: 919-931.
45. Hadas O, Pinkas R & Erez J (2001) High chemoautotrophic primary production in Lake Kinneret, Israel: A neglected link in the carbon cycle of the lake. Limnol Oceanogr 46: 1968-1976.
46. Hahn MW, Lang E, Brandt U, Wu QL & Scheuerl T (2009) Emended description of the genus Polynucleobacter and the species Polynucleobacter necessarius and proposal of two subspecies, P. necessarius subsp. necessarius subsp. nov. and P. necessarius subsp. asymbioticus subsp. nov. Int J Syst Evol Micr 59: 2002-2009.
47. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
48. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM & DeLong EF (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biology 4: e95.
49. Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C, Pernthaler A & Pernthaler J (2005) Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microb 71: 2303-2309.
50. Hinrichs KU & Boetius A (2002) The anaerobic oxidation of methane: new insights in microbial ecology and biogeochemistry. Ocean Margin Systems (Wefer G, Billet D, Hebbeln D, Jørgensen BB, Schlüter M & Van Weering TC, eds), pp. 457-477. Springer-Verlag, Heidelberg.
51. Holmer M & Storkholm P (2001) Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwater Biol 46: 431-451.
52. Huber T, Faulkner G & Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
53. Inagaki F, Suzuki M, Takai K et al. (2003) Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microb 69: 7224-7235.
54. Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM, Druffel ER & Pearson A (2006) Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. P Natl Acad Sci USA 103: 6442-6447.
55. Jezberova J, Jezbera J, Brandt U, Lindstrom ES, Langenheder S & Hahn MW (2010) Ubiquity of Polynucleobacter necessarius ssp. asymbioticus in lentic freshwater habitats of a heterogeneous 2000km area. Environ Microbiol 12: 658-669.
56. Jones WJ, Nagle DP Jr. & Whitman WB (1987) Methanogens and the diversity of archaebacteria. Microbiol Rev 51: 135-177.
57. Jorgensen BB, Kuenen JG & Cohen Y (1979) Microbial transformation of sulfur compounds in a stratified lake (Solar Lake, Sinai). Limnol Oceanogr 24: 799-822.
58. Jost G, Martens-Habbena W, Pollehne F, Schnetger B & Labrenz M (2010) Anaerobic sulfur oxidation in the absence of nitrate dominates microbial chemoautotrophy beneath the pelagic chemocline of the eastern Gotland Basin, Baltic Sea. FEMS Microbiol Ecol 71: 226-236.
59. Kallistova A, Kevbrina MV, Pimenov NV, Rusanov II, Rogozin D, Wehrli B & Nozhevnikova AN (2006) Sulfate reduction and methanogenesis in the Shira and Shunet meromictic lakes (Khakass Republic, Russia). Mikrobiologiia 75: 828-835.
60. Kirchman DL, Elifantz H, Dittel AI, Malmstrom RR & Cottrell MT (2007) Standing stocks and activity of Archaea and Bacteria in the western Arctic Ocean. Limnol Oceanogr 52: 495-507.
61. Klammer S, Posch T, Sonntag B, Griebler C, Mindl B & Psenner R (2002) Dynamics of bacterial abundance, biomass, activity, and community composition in the oligotrophic Traunsee and the Traun river (Austria). Water Air Soil Poll 2: 137-163.
62. Kletzin A, Urich T, Muller F, Bandeiras TM & Gomes CM (2004) Dissimilatory oxidation and reduction of elemental sulfur in thermophilic archaea. J Bioenerg Biomembr 36: 77-91.
63. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB & Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546.
64. Llirós M, Casamayor EO & Borrego C (2008) High archaeal richness in the water column of a freshwater sulfurous karstic lake along an interannual study. FEMS Microbiol Ecol 66: 331-342.
65. Llirós M, Gich F, Plasencia A et al. (2010) Vertical distribution of ammonia-oxidizing crenarchaeota and methanogens in the epipelagic waters of Lake Kivu. Appl Environ Microb 76: 6853-6863.
66. Lovley DR & Klug MJ (1983) Sulfate reducers can outcompete methanogens at freshwater sulfate concentrations. Appl Environ Microb 45: 187-192.
67. Ludwig W, Strunk O, Westram R et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
68. Manz W, Amann R, Ludwig W, Vancanneyt M & Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142: 1097-1106.
69. Margalef R (1982) Ecología. Omega, Barcelona.
70. Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR & Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461: 976-979.
71. Muyzer G & Ramsing NB (1995) Molecular methods to study the organization of microbial communities. Water Sci Technol 32: 1-9.
72. Ouverney CC & Fuhrman JA (2000) Marine planktonic archaea take up amino acids. Appl Environ Microb 66: 4829-4833.
73. Overmann J (2006) The family Chlorobiaceae. The Prokaryotes: A Handbook on the Biology of Bacteria, Vol. 7 (Dworkin M, Falkow S, Rosenberg E, Schleifer KH & Stackebrandt E, eds), pp. 359-378. Springer, Heidelberg.
74. Parkes RJ, Webster G, Cragg BA et al. (2005) Deep sub-seafloor prokaryotes stimulated at interfaces over geological time. Nature 436: 390-394.
75. Pedrós-Alió C & Guerrero R (1991) Abundance and activity of bacterioplankton in warm lakes. Verh Int Verein Limnol 24: 1212-1219.
76. Pedrós-Alió C, García-Cantizano J & Calderón Paz JI (1993) Bacterial production in anarobic water columns. Current Methods in Aquatic Microbial Ecology (Kempf PF, Sherr BF, Sherr EB & Cole JJ, eds), pp. 519-530. Lewis, Boca Ratón, FL.
77. Pérez MT, Pausz C & Herndl GJ (2003) Major shift in bacterioplankton utilization of enantiomeric aminoacids between surface waters and the ocean's interior. Limnol Oceanogr 48: 755-763.
78. Pernthaler A, Pernthaler J & Amann R (2002) Fluorescence in situ hybridization and catalyzed reported deposition for the identification of marine bacteria. Appl Environ Microb 68: 3094-4101.
79. Raskin L, Stromley JM, Rittmann BE & Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microb 60: 1232-1240.
80. Robertson CE, Harris JK, Spear JR & Pace NR (2005) Phylogenetic diversity and ecology of environmental Archaea. Curr Opin Microbiol 8: 638-642.
81. 2 assimilation as a measure of metabolic activity in planktonic and sessile bacteria. J Microbiol Meth 59: 381-393.
82. Ryan MP, Pembroke JT & Adley CC (2007) Ralstonia pickettii in environmental biotechnology: potential and applications. J Appl Microbiol 103: 754-764.
83. Saitou N & Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
84. Schleper C, Jurgens G & Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3: 479-488.
85. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75: 7537-7541.
86. Schouten S, Hopmans EC, Pancost RD & Sinninghe Damsté J (2000) Widespread occurrence of structurally diverse tetraether membrane lipids: evidence for the ubiquitous presence of low-temperature relatives of hyperthermophiles. P Natl Acad Sci USA 97: 14421-14426.
87. Schouten S, Hopmans EC, Baas M et al. (2008) Intact membrane lipids of 'Candidatus Nitrosopumilus maritimus, ' a cultivated representative of the cosmopolitan mesophilic group I Crenarchaeota. Appl Environ Microb 74: 2433-2440.
88. Shively JM, van Keulen G & Meijer WG (1998) Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu Rev Microbiol 52: 191-230.
89. Simpson PG & Whitman WB (1993) Anabolic pathways in methanogens. Methanogenesis: Ecology, Physiology, Biochemistry and Genetics (Ferry JG, ed), pp. 445-472. Chapman & Hall Inc., New York.
90. Sinke AJC, Cornelese AA, Cappenberg TE & Zehnder AJB (1992) Seasonal variation in sulfate reduction and methanogenesis in peaty sediments of eutrophic Lake Loosdrecht, The Netherlands. Biogeochemistry 16: 43-61.
91. Sinninghe Damste JS, Rijpstra WI, Hopmans EC, Prahl FG, Wakeham SG & Schouten S (2002) Distribution of membrane lipids of planktonic Crenarchaeota in the Arabian Sea. Appl Environ Microb 68: 2997-3002.
92. Takai K, Moser DP, DeFlaun M, Onstott TC & Fredrickson JK (2001) Archaeal diversity in waters from deep South African gold mines. Appl Environ Microb 67: 5750-5760.
93. Teske A & Sorensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2: 3-18.
94. Varela MM, van Aken HM, Sintes E & Herndl GJ (2008) Latitudinal trends of Crenarchaeota and Bacteria in the meso- and bathypelagic water masses of the Eastern North Atlantic. Environ Microbiol 10: 110-124.
95. Walker CB, de la Torre JR, Klotz MG et al. (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. P Natl Acad Sci USA 107: 8818-8823.
96. Watanabe K, Komatsu N, Ishii Y & Negishi M (2009) Effective isolation of bacterioplankton genus Polynucleobacter from freshwater environments grown on photochemically degraded dissolved organic matter. FEMS Microbiol Ecol 67: 57-68.
97. Wuchter C, Schouten S, Boschker HT & Sinninghe Damste JS (2003) Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol Lett 219: 203-207.
98. Yakimov MM, La Cono V & Denaro R (2009) A first insight into the occurrence and expression of functional amoA and accA genes of autotrophic and ammonia-oxidizing bathypelagic Crenarchaeota of Tyrrhenian Sea. Deep-Sea Res II 56: 748-754.