Advertisement

A Random Biogeochemical Walk into Three Soda Lakes of the Western USA: With an Introduction to a Few of Their Microbial Denizens

  • Ronald S. OremlandEmail author
Chapter
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 27)

Abstract

Soda lakes are by definition both saline and alkaline, thereby immediately fulfilling the basic requirements of an environment exhibiting multiple forms of extreme conditions to which the biota are routinely exposed. Herein I will discuss three closed basin soda lakes located in Nevada (Big Soda Lake) and California (Mono and Searles Lakes) that have been investigated over the past three decades. While they represent extreme environments in these two primary dimensions, they are augmented in this category by considerations of their natural abundances of toxic elements (i.e., arsenic and boron), their paucity of important divalent cations (i.e., magnesium and calcium), the presence of hot spring microbial niches in their basins, and the perennial or occasional occurrences of meromixis, a hydrological stratification feature that results in exceptionally high levels of sulfide occurring in their hypolimnia. I will also discuss the microbes and microbial processes observed in these lakes and how they are adapted to some of the above-mentioned extreme conditions.

Keywords

Sulfate Reduction Glycine Betaine Soda Lake Mono Lake Arsenate Reductase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Afkar E, Lisak J, Saltikov C, Basu P, Oremland RS, Stolz JF (2003) The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiol Lett 226:107–112PubMedCrossRefGoogle Scholar
  2. Baesman SM, Bullen TD, Dewald J, Zhang DH, Curran S, Islam FS, Beveridge TJ, Oremland RS (2007) Formation of tellurium nanocrystals during anaerobic growth of bacteria that use Te oxyanions as respiratory electron acceptors. Appl Environ Microbiol 73:2135–2143PubMedCrossRefGoogle Scholar
  3. Baesman SM, Stolz JF, Kulp TR, Oremland RS (2009) Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles 13:695–705PubMedCrossRefGoogle Scholar
  4. Baross JA, Dahm CN, Ward AK, Lilley MD, Sedell R (1982) Initial microbiological response in lakes to the Mt. St. Helens eruption. Nature 296:49–52CrossRefGoogle Scholar
  5. Basturea GN, Harris TK, Deutscher MP (2012) Growth of a bacterium that apparently uses arsenic instead of phosphorus is a consequence of massive ribosome breakdown. J Biol Chem 287:28816–28819PubMedCrossRefGoogle Scholar
  6. Carini SA, Joye SB (2008) Nitrification in Mono Lake, California (USA): activity and community composition during contrasting hydrological regimes. Limnol Oceanogr 53:2546–2557CrossRefGoogle Scholar
  7. Carini SA, LeCleir G, Bano S, Joye SB (2005) Activity, abundance and diversity of aerobic methanotrophs in an alkaline, hypersaline lake (Mono Lake, CA, USA). Environ Microbiol 7:1127–1138PubMedCrossRefGoogle Scholar
  8. Christensen MN, Gilbert CM, Lajoie KR, Al Rawi Y (1969) Geological – geophysical interpretation of the Mono Basin, California-Nevada. J Geophys Res 74:5221–5239CrossRefGoogle Scholar
  9. Cloern JE, Cole B, Oremland RS (1983a) Seasonal changes in the chemical and biological nature of a meromictic lake (Big Soda Lake, Nevada, USA). Hydrobiologia 105:195–206CrossRefGoogle Scholar
  10. Cloern JE, Cole B, Oremland RS (1983b) Autotrophic processes in meromictic Big Soda Lake, Nevada. Limnol Oceanogr 28:1049–1061CrossRefGoogle Scholar
  11. Cloern JE, Cole BE, Wienke SM (1987) Big Soda Lake (Nevada). 4. Vertical fluxes of particulate matter: seasonality and variations across the chemocline. Limnol Oceanogr 32:804–814CrossRefGoogle Scholar
  12. Cohen Y, Krumbein WE, Goldberg M, Shilo M (1977) Solar Lake (Sinai). 1. Physical and chemical limnology. Limnol Oceanogr 22:597–608CrossRefGoogle Scholar
  13. Connell TL, Joye SB, Miller LG, Oremland RS (1997) Bacterial oxidation of methyl bromide in Mono Lake, California. Environ Sci Technol 31:1489–1495CrossRefGoogle Scholar
  14. Dana G, Herbst DB, Lovejoy C, Loeffler RM, Otsuki K (1977) Physical and chemical limnology. In: Winkler DW (ed) An ecological study of Mono Lake, California, vol 12, Institute of Ecology Publication. University of California, Davis, pp 40–42Google Scholar
  15. Erb TJ, Kiefer P, Hattendorf B, Günther D, Vorholt JA (2012) GFAJ-1 is an arsenate-resistant, phosphate-dependent organism. Science 337:467–469PubMedCrossRefGoogle Scholar
  16. Felmy AR, Weare JH (1986) The prediction of borate mineral equilibria in natural waters: application to Searles Lake, California. Geochim Cosmochim Acta 50:2771–2783CrossRefGoogle Scholar
  17. Hill DP, Bailey RA, Ryall AS (1985) Active tectonic and magmatic processes beneath Long Valley Caldera, eastern California: an overview. J Geophys Res 90:11,111–11,120Google Scholar
  18. Hoeft SE, Lucas F, Hollibaugh JT, Oremland RS (2002) Characterization of microbial arsenate reduction in the anoxic bottom waters of Mono Lake, California. Geomicrobiol J 19:23–40CrossRefGoogle Scholar
  19. Hoeft SE, Kulp TR, Stolz JF, Hollibaugh JT, Oremland RS (2004) Dissimilatory arsenate reduction with sulfide as the electron donor: experiments with Mono Lake water and isolation of strain MLMS-1, a chemoautotrophic arsenate-respirer. Appl Environ Microbiol 70:2741–2747PubMedCrossRefGoogle Scholar
  20. Hoeft SE, Switzer Blum J, Stolz JF, Tabita FR, Witte B, King GM, Santini JM, Oremland RS (2007) Alkalilimnicola ehrlichii, sp. nov., a novel, arsenite-oxidizing haloalkaliphilic -Proteobacterium capable of chemoautotrophic or heterotrophic growth with nitrate or oxygen as the electron acceptor. Int J Syst Evol Microbiol 57:504–512PubMedCrossRefGoogle Scholar
  21. Hoeft SE, Kulp TR, Han S, Lanoil B, Oremland RS (2010) Coupled arsenotrophy in a photosynthetic hot spring biofilm from Mono Lake, California. Appl Environ Microbiol 76:4633–4639PubMedCrossRefGoogle Scholar
  22. Hollibaugh JT, Carini S, Gürleyük H, Jellison R, Joye SB, Lecleir G, Meile C, Vasquez L, Wallschläger D (2005) Distribution of arsenic species in alkaline, hypersaline, Mono Lake, California and response to seasonal stratification and anoxia. Geochim Cosmochim Acta 69:1925–1937CrossRefGoogle Scholar
  23. Hollibaugh JT, Budinoff C, Hollibaugh RA, Ransom B, Bano N (2006) Sulfide oxidation coupled to arsenate reduction by a diverse microbial community in a soda lake. Appl Environ Microbiol 72:2043–2049PubMedCrossRefGoogle Scholar
  24. Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69:1030–1042PubMedCrossRefGoogle Scholar
  25. Iversen N, Oremland RS, Klug MJ (1987) Big Soda Lake (Nevada). 3. Pelagic methanogenesis and anaerobic methane oxidation. Limnol Oceanogr 32:804–814CrossRefGoogle Scholar
  26. Jellison R, Melack JM (1993) Meromixis in hypersaline Mono Lake, California. 1. Stratification and vertical mixing during onset, persistence, and breakdown of meromixis. Limnol Oceanogr 38:1008–1019CrossRefGoogle Scholar
  27. Jellison R, Miller LG, Melack JM, Dana GL (1993) Meromixis in hypersaline Mono Lake, California. 2. Nitrogen fluxes. Limnol Oceanogr 38:1020–1039CrossRefGoogle Scholar
  28. Johannesson KH, Lyons WB (1994) The rare earth element geochemistry of Mono Lake water and the importance of carbonate complexing. Limnol Oceanogr 39:1141–1154CrossRefGoogle Scholar
  29. Jørgensen BB, Cohen Y (1977) Solar Lake (Sinai). 5. The sulfur cycle of the benthic cyanobacterial mats. Limnol Oceanogr 22:657–666CrossRefGoogle Scholar
  30. Joye SB, Connell TL, Miller LG, Jellison R, Oremland RS (1999) Oxidation of ammonia and methane in an alkaline, saline lake. Limnol Oceanogr 44:178–188CrossRefGoogle Scholar
  31. Kang Y-S, Heinemann J, Bothner B, Rensing C, McDermott TR (2012) Integrated co-regulation of bacterial arsenic and phosphorus metabolism. Environ Microbiol 14(12):3097–3109PubMedCrossRefGoogle Scholar
  32. Kharaka YK, Robinson SW, Law LM, Carothers WW (1984) Hydrogeochemistry of Big Soda Lake, Nevada: an alkaline meromictic desert lake. Geochim Cosmochim Acta 48:823–835CrossRefGoogle Scholar
  33. Kiene R, Oremland RS, Catena A, Miller L, Capone DG (1986) Metabolism of reduced methylated sulfur compounds in anaerobic sediments and by a pure culture of an estuarine methanogen. Appl Environ Microbiol 52:1037–1045PubMedGoogle Scholar
  34. Kim E-H, Rensing C (2012) Genome of Halomonas strain GFAJ-1, a blueprint for fame or business as usual. J Bacteriol 194:1643–1645PubMedCrossRefGoogle Scholar
  35. Kimmel BL, Gersberg RM, Axler RP, Goldman CR (1978) Recent changes in the meromictic status of Big Soda Lake, Nevada. Limnol Oceanogr 23:1021–1025CrossRefGoogle Scholar
  36. King GM (1984) Utilization of hydrogen, acetate and “non-competitive” substrates by methanogenic bacteria in marine sediments. Geomicrobiol J 3:275–306CrossRefGoogle Scholar
  37. Kulp TR, Hoeft SE, Miller LG, Saltikov C, Nilsen J, Han S, Lanoil B, Oremland RS (2006) Dissimilatory arsenate- and sulfate-reduction in sediments of two hypersaline, arsenic-rich soda lakes: Mono and Searles Lakes, California. Appl Environ Microbiol 72:6514–6526PubMedCrossRefGoogle Scholar
  38. Kulp TR, Han S, Saltikov C, Lanoil B, Zargar K, Oremland RS (2007) Effects of imposed salinity gradients on dissimilatory arsenate-reduction, sulfate-reduction, and other microbial processes in sediments from two California soda lakes. Appl Environ Microbiol 73:5130–5137PubMedCrossRefGoogle Scholar
  39. Kulp TR, Hoeft SE, Asao M, Madigan MT, Hollibaugh JT, Fisher JC, Stolz JF, Culbertson CW, Miller LG, Oremland RS (2008) Arsenic(III) fuels anoxygenic photosynthesis in hot spring biofilms from Mono Lake, California. Science 321:967–970PubMedCrossRefGoogle Scholar
  40. Laverman AM, Switzer Blum J, Schaeffer JK, Philips EJ, Lovley DR, Oremland RS (1995) Growth of strain SES-3 with arsenate and other diverse electron acceptors. Appl Environ Microbiol 61:3556–3561PubMedGoogle Scholar
  41. Lin J-L, Joye SB, Schafer H, Scholten JCM, McDonald IR, Murrell JC (2005) Diversity of methanotrophs in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 71:6458–6462PubMedCrossRefGoogle Scholar
  42. Lonsdale P (1977) Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep-Sea Res 24:857–863CrossRefGoogle Scholar
  43. Mason DT (1967) Limnology of Mono Lake, California. PhD dissertation, University of California, BerkeleyGoogle Scholar
  44. Miller LG, Oremland RS (2008) Electricity generation by anaerobic bacteria and anoxic sediments from hypersaline soda lakes. Extremophiles 12:837–848PubMedCrossRefGoogle Scholar
  45. Miller LG, Oremland RS, Paulsen S (1986) Measurement of N2O reductase activity in aquatic sediments. Appl Environ Microbiol 51:18–24PubMedGoogle Scholar
  46. Miller LG, Jellison R, Oremland RS, Culbertson CW (1993) Meromixis in hypersaline Mono Lake, California. 3. Biogeochemical response to stratification and overturn. Limnol Oceanogr 38:1040–1051CrossRefGoogle Scholar
  47. Nercessian O, Kalyuzhnaya MG, Joye SB, Lidstrom ME, Chistoserdova L (2006) Analysis of fae and fhcD genes in Mono Lake, California. Appl Environ Microbiol 71:8949–8953CrossRefGoogle Scholar
  48. Oremland RS (1983) Hydrogen metabolism by decomposing cyanobacterial aggregates in Big Soda Lake, Nevada. Appl Environ Microbiol 45:1519–1525PubMedGoogle Scholar
  49. Oremland RS (1990) Nitrogen fixation dynamics of two diazotrophic communities in Mono Lake, California. Appl Environ Microbiol 56:614–622PubMedGoogle Scholar
  50. Oremland RS, DesMarais DJ (1983) Distribution, abundance and carbon isotopic composition of gaseous hydrocarbons in Big Soda Lake, Nevada: an alkaline, moderately hypersaline desert lake. Geochim Cosmochim Acta 47:355–371CrossRefGoogle Scholar
  51. Oremland RS, King GM (1989) Methanogenesis in hypersaline environments. In: Cohen Y, Rosenberg E (eds) Microbial mats: physiological ecology of benthic microbial communities. American Society for Microbiology, Washington, DC, pp 180–189Google Scholar
  52. Oremland RS, Miller LG (1993) Biogeochemistry of natural gases in three alkaline, permanently stratified (meromictic) lakes. In: Howell D (ed) Future of energy gases. USGS professional paper. U.S. Government Printing Office, Washington, DC, pp 439–452Google Scholar
  53. Oremland RS, Polcin S (1982) Methanogenesis and sulfate-reduction: competitive and noncompetitive substrates in estuarine sediments. Appl Environ Microbiol 44:1270–1276PubMedGoogle Scholar
  54. Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944PubMedCrossRefGoogle Scholar
  55. Oremland RS, Marsh L, DesMarais DJ (1982a) Methanogenesis in Big Soda Lake, Nevada: an alkaline, moderately hypersaline desert lake. Appl Environ Microbiol 43:462–468PubMedGoogle Scholar
  56. Oremland RS, Marsh LM, Polcin S (1982b) Methane production and simultaneous sulfate-reduction in anoxic, salt marsh sediments. Nature 296:143–145CrossRefGoogle Scholar
  57. Oremland RS, Miller L, Whiticar M (1987) Sources and flux of natural gases from Mono Lake, California. Geochim Cosmochim Acta 51:2915–2929CrossRefGoogle Scholar
  58. Oremland RS, Whiticar MJ, Strohmaier FE, Kiene RP (1988) Bacterial ethane formation from reduced, ethylated sulfur compounds in anoxic sediments. Geochim Cosmochim Acta 52:1895–1904CrossRefGoogle Scholar
  59. Oremland RS, Miller LG, Culbertson CW, Robinson S, Smith RL, Lovley DR, Whiticar MJ, King GM, Kiene RP, Iversen N, Sargent M (1993) Aspects of the biogeochemistry of methane in Mono Lake and the Mono Basin of California, USA. In: Oremland RS (ed) The biogeochemistry of global change: radiative trace gases. Chapman & Hall, New York, pp 704–744CrossRefGoogle Scholar
  60. Oremland RS, Switzer Blum J, Culbertson CW, Visscher PT, Miller LG, Dowdle P, Strohmaier FE (1994) Isolation, growth and metabolism of an obligately anaerobic, selenate-respiring bacterium, strain SES-3. Appl Environ Microbiol 60:3011–3019PubMedGoogle Scholar
  61. Oremland RS, Dowdle PR, Hoeft S, Sharp JO, Schaefer JK, Miller LG, Switzer Blum J, Smith RL, Bloom NS, Wallschlaeger D (2000) Bacterial dissimilatory reduction of arsenate and sulfate in meromictic Mono Lake, California. Geochim Cosmochim Acta 64:3073–3084CrossRefGoogle Scholar
  62. Oremland RS, Hoeft SE, Bano N, Hollibaugh RA, Hollibaugh JT (2002) Anaerobic oxidation of arsenite in Mono Lake water and by a facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Appl Environ Microbiol 68:4795–4802PubMedCrossRefGoogle Scholar
  63. Oremland RS, Stolz JF, Hollibaugh JT (2004) The microbial arsenic cycle in Mono Lake, California. FEMS Microbiol Ecol 48:15–27PubMedCrossRefGoogle Scholar
  64. Oremland RS, Kulp TR, Switzer Blum J, Hoeft S, Baesman S, Miller LG, Stolz JF (2005) A microbial arsenic cycle in a salt-saturated, extreme environment. Science 308:1305–1308PubMedCrossRefGoogle Scholar
  65. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedGoogle Scholar
  66. Oren A (2011) Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923PubMedCrossRefGoogle Scholar
  67. Oren A (2013) Two centuries of microbiological research in the Wadi Natrun, Egypt: a model system for the study of the ecology, physiology, and taxonomy of haloalkaliphilic microorganisms. In: Seckbach J, Oren A, Stan-Lotter H (eds) Polyextremophiles: life under multiple forms of stress. Springer, Dordrecht, pp 103–119Google Scholar
  68. Phung LT, Silver S, Trimble WL, Gilbert JA (2012) Draft genome of Halomonas species strain GFAJ-1 (ATCC BAA-2256). J Bacteriol 194:1835–1836CrossRefGoogle Scholar
  69. Priscu JC, Axler RP, Carlton RG, Reuter JE, Arneson PA, Goldman CR (1982) Vertical profiles of primary production, biomass and physico-chemical properties in meromictic Big Soda Lake, Nevada, U.S.A. Hydrobiology 96:113–120CrossRefGoogle Scholar
  70. Reaves ML, Sinha S, Rabinowitz JD, Kruglyak L, Redfield RJ (2012) Absence of detectable arsenate in DNA from arsenate-grown GFAJ-1 cells. Science 337:470–473PubMedCrossRefGoogle Scholar
  71. Reed WE (1977) Biogeochemistry of Mono Lake, California. Geochim Cosmochim Acta 41:1231–1245CrossRefGoogle Scholar
  72. Richey C, Chovanec P, Hoeft SE, Oremland RS, Basu P, Stolz JF (2009) Respiratory arsenate reductase as a bidirectional enzyme. Biochem Biophys Res Commun 382:298–302CrossRefGoogle Scholar
  73. Roesler CS, Culbertson CW, Etheridge SM, Goericke R, Kiene RP, Miller LG, Oremland RS (2002) Distribution, production, and ecophysiology of Picocycstis strain ML in Mono Lake, CA. Limnol Oceanogr 47:440–452CrossRefGoogle Scholar
  74. Rosen BP, Ajees AA, McDermott TR (2011) Life and death with arsenic. Arsenic life: an analysis of the recent report “A bacterium that can grow using arsenic instead of phosphorus”. Bioessays 33:350–357PubMedCrossRefGoogle Scholar
  75. Rush FE (1972) Hydrologic reconnaissance of Big and Little Soda Lakes, Churchill County, Nevada. Water resources – information. Series report II, Department of Conservation and National Resources, Nevada, 2 ppGoogle Scholar
  76. Scholten JCM, Joye SB, Hollibaugh JT, Murrell C (2005) Molecular analysis of the sulfate reducing and methanogenic community in a meromictic lake (Mono Lake, California) by targeting 16SrRNA, methyl CoM-, APS- and DSR-genes. Microb Ecol 50:29–39PubMedCrossRefGoogle Scholar
  77. Silver S, Phung LT (2011) Novel expansion of living chemistry or just a serious mistake? FEMS Microbiol Lett 315:79–80PubMedCrossRefGoogle Scholar
  78. Smith GI (1979) Subsurface stratigraphy and geochemistry of late Quaternary evaporites, Searles Lake, California. U.S. Geological Survey Professional Paper 1043. U.S. Government Printing Office, Washington, DC, pp 1–130Google Scholar
  79. Smith RL, Oremland RS (1987) Big Soda Lake (Nevada). 2. Pelagic sulfate reduction. Limnol Oceanogr 32:794–803CrossRefGoogle Scholar
  80. Sorokin DY, Kuenen JG, Muyzer G (2011) The microbial sulfur cycle at extremely haloalkaline conditions of soda lakes. Front Microbiol 2:44PubMedCrossRefGoogle Scholar
  81. Stine S (1990) Late Holocene fluctuations of Mono Lake, eastern California. Palaeogeogr Palaeoclimatol Palaeoecol 578:333–381CrossRefGoogle Scholar
  82. Stolz JF, Ellis DJ, Switzer Blum J, Ahmann D, Oremland RS, Lovley DR (1999) Sulfurospirillum barnesii sp. nov., Sulfurospirillum arsenophilus sp. nov., and the Sulfurospirillum clade in the -Proteobacteria. Int J Syst Bacteriol 49:1177–1180PubMedCrossRefGoogle Scholar
  83. Switzer Blum J, Burns Bindi A, Buzzelli J, Stolz JF, Oremland RS (1998) Bacillus arsenicoselenatis sp. nov., and Bacillus selenitireducens sp. nov.: two haloalkaliphiles from Mono Lake, California which respire oxyanions of selenium and arsenic. Arch Microbiol 171:19–30PubMedCrossRefGoogle Scholar
  84. Switzer Blum J, Han S, Lanoil B, Saltikov C, Witte B, Tabita FR, Langley S, Beveridge TJ, Stolz JF, Jahnke L, Oremland RS (2009) Halarsenatibacter silvermanii strain SLAS-1, gen. nov., sp. nov., ecophysiology of an extremely halophilic, facultative chemoautotrophic arsenate-respirer from Searles Lake, California. Appl Environ Microbiol 75:1950–1960CrossRefGoogle Scholar
  85. Switzer Blum J, Kulp TR, Han S, Lanoil B, Saltikov CW, Stolz JF, Miller LG, Oremland RS (2012) Desulfohalophilus alkaliarsenatis gen. nov., sp. nov., an extremely halophilic sulfate- and arsenate-respiring bacterium from Searles Lake, California. Extremophiles 16:727–742CrossRefGoogle Scholar
  86. Ward BB, Martino D, Diaz C, Joye SB (2000) Analysis of ammonia-oxidizing bacteria from hypersaline Mono Lake, California on the basis of 16S rRNA sequences. Appl Environ Microbiol 66:2873–2881PubMedCrossRefGoogle Scholar
  87. Wolfe-Simon F, Blum JS, Kulp TR, Gordon GW, Hoeft SE, Stolz JM, Webb SM, Davies PCW, Anbar AD, Oremland RS (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science 332:1163–1166PubMedCrossRefGoogle Scholar
  88. Zargar K, Hoeft S, Oremland R, Saltikov CW (2010) Genetic identification of a novel arsenite oxidase, arxA, in the haloalkaliphilic, arsenite oxidizing bacterium Alkalilimnicola ehrlichii strain MLHE-1. J Bacteriol 192:3755–3762PubMedCrossRefGoogle Scholar
  89. Zargar KA, Conrad A, Bernick DL, Lowe TM, Stolc V, Hoeft S, Oremland RS, Stolz J, Saltikov CW (2012) ArxA, a new clade of arsenite oxidase within the DMSO reductase family of molybdenum oxidoreductases. Environ Microbiol 14(7):1635–1645PubMedCrossRefGoogle Scholar
  90. Zehr JP, Harvey RW, Oremland RS, Cloern JE, George L, Lane JL (1987) Big Soda Lake (Nevada). 1. Pelagic bacterial heterotrophy and biomass. Limnol Oceanogr 32:781–793CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.U.S. Geological SurveyMenlo ParkUSA

Personalised recommendations