Microbiology of Lonar Lake and other soda lakes

ISME Journal

Volumn 7, Issue 3, 2013, Pages 468-476

  Antony, Chakkiath Paul ^a   Kumaresan, Deepak ^b   Hunger, Sindy ^c   Drake, Harold L ^c   Murrell, J Colin ^d   Shouche, Yogesh S ^a  

^a NATIONAL CENTRE FOR CELL SCIENCE   (India)

^b CSIRO   (Australia)

^c UNIVERSITY OF BAYREUTH   (Germany)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

alkaliphiles; Lonar Lake; microbial prospecting; soda lakes; stable isotope probing

Indexed keywords

ALKALINE WATER; ANTHROPOGENIC EFFECT; BACTERIUM; FOOD WEB; GROWTH RATE; PHYSICOCHEMICAL PROPERTY; PROKARYOTE; SALINE LAKE;

ARCHAEON; BACTERIAL PHENOMENA AND FUNCTIONS; BIODIVERSITY; BIOTECHNOLOGY; ECOSYSTEM; INDIA; LAKE; MICROBIOLOGY; PHYSIOLOGY; REVIEW;

ARCHAEA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIODIVERSITY; BIOTECHNOLOGY; ECOSYSTEM; INDIA; LAKES;

EAST AFRICAN RIFT; INDIA; LONAR LAKE; MAHARASHTRA;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 84876486228     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.137     Document Type: Review

References (82)

1. Andersen GL, He Z, Desantis TZ, Brodie EL, Zhou J. (2010). The use of microarrays in microbial ecology. In: Liu WT, Jansson JK (eds). Environmental Molecular Microbiology. Caister Academic Press: Norwich, pp. 87-110.
2. Antony CP, Kumaresan D, Ferrando L, Boden R, Moussard H, Scavino AF et al. (2010). Active methylotrophs in the sediments of Lonar Lake, a saline and alkaline ecosystem formed by meteor impact. ISMEJ4: 1470-1480.
3. Antony CP, Doronina NV, Boden R, Trotsenko YA, Shouche YS, Murrell JC. (2012a). Methylophaga lonarensis, a novel moderately haloalkaliphilic methylotroph isolated from the soda lake sediments of a meteorite impact crater. Int J Syst Evol Microbiol 62: 1613-1618.
4. Antony CP, Murrell JC, Shouche YS. (2012b). Molecular diversity of methanogens and identification of Metha-nolobus sp. as active methylotrophic Archaea in Lonar crater lake sediments. FEMS Microbiol Ecol 81: 43-51.
5. Asao M, Pinkart HC, Madigan MT. (2011). Diversity of extremophilic purple phototrophic bacteria in Soap Lake, a Central Washington (USA) Soda Lake. Environ Microbiol 13: 2146-2157.
6. Cadillo-Quiroz H, Yashiro E, Yavitt JB, Zinder SH. (2008). Characterization of the archaeal community in a minerotrophic fen and terminal restriction fragment length polymorphism-directed isolation of a novel hydrogenotrophic methanogen. Appl Environ Microbiol 74: 2059-2068. (Pubitemid 351522059)
7. Carini SA, Joye SB. (2008). Nitrification in Mono Lake, California: Activity and community composition during contrasting hydrological regimes. Limnol Ocea-nogr 53: 2546-2557.
8. Chakravarty I. (2009). Conservation and management for the Lonar crater-lake, Maharashtra, India. S Asian J Tour Herit 2: 112-118.
9. Ciulla RA, Diaz MR, Taylor BF, Roberts MF. (1997). Organic osmolytes in aerobic bacteria from Mono Lake, an alkaline, moderately hypersaline environment. Appl Environ Microbiol 63: 220-226. (Pubitemid 27020393)
10. Couradeau E, Benzerara K, Gerard E, Moreira D, Bernard S, Brown GE Jr, Lopez-Garcia P. (2012). An early-branching microbialite cyanobacterium forms intracellular carbonates. Science 336: 459-462.
11. Dedysh SN, Pankratov TA, Belova SE, Kulichevskaya IS, Liesack W. (2006). Phylogenetic analysis and in situ identification of bacteria community composition in an acidic Sphagnum peat bog. Appl Environ Microbiol 72: 2110-2117.
12. Doronina NV, Darmaeva T, Trotsenko YA. (2001). New aerobic methylotrophic isolates from the Soda lakes of the southern Transbaikal. Mikrobiologiia 70: 398-404. (Pubitemid 33772260)
13. Doronina NV, Darmaeva TD, Trotsenko YA. (2003). Methylophaga alcalica sp. nov., a novel alkaliphilic and moderately halophilic, obligately methylotrophic bacterium from an East Mongolian saline soda lake. Int J Syst Evol Microbiol 53: 223-229. (Pubitemid 36285244)
14. Drake HL, Gofiner AS, Daniel SL. (2008). Old acetogens, new light. In: Wiegel J, Maier RJ, Adams MWW (eds). Incredible Anaerobes: From Physiology to Genomics to Fuels. New York Academy of Sciences: Boston, MA, pp. 100-128. (Pubitemid 351451162)
15. Drake HL, Horn MA, Wüst PK. (2009). Intermediary ecosystem metabolism as a main driver of methano-genesis in acidic wetland soil. Environ Microbiol Rep 1: 307-318.
16. Duckworth AW, Grant WD, Jones BE, Van Steenbergen R. (1996). Phylogenetic diversity of soda lake alkali-philes. FEMS Microbiol Ecol 19: 181-191. (Pubitemid 26178365)
17. Foti M, Sorokin DY, Lomans B, Mussman M, Zakharova EE, Pimenov NV et al. (2007). Diversity, activity and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl Environ Microbiol 73: 2093-2100. (Pubitemid 46649498)
18. Fredriksson K, Dube A, Milton DJ, Balasundaram MS. (1973). Lonar Lake, India: an impact crater in basalt. Science 180: 862-864.
19. Gebre-Mariam Z. (1998). Human interactions and water quality in the Horn of Africa. In: Schoneboom J (eds). Science in Africa-Emerging Water Management Problems. A Publication of the Symposium at the American Association for the Advancement of Science (AAAS), Annual Meeting 1998: Philadelphia, pp 47-61.
20. Giri BJ, Bano N, Hollibaugh JT. (2004). Distribution of RuBisco genotypes along a redox gradient in Mono Lake, California. Appl Environ Microbiol 70: 3443-3448. (Pubitemid 38745889)
21. Grant WD, Jones BE, Mwatha WE. (1990). Alkaliphiles: ecology, diversity and applications. FEMS Microbiol Rev 75: 255-270.
22. Grant WD. (1992). Alkaline environments. In: Lederberg J (ed.). Encyclopaedia of Microbiology, 1st edn. Academic Publishers: London, pp. 73-80.
23. Grant S, Grant WD, Jones BE, Kato C, Li L. (1999). Novel archaeal phytotypes from an East African alkaline saltern. Extremophiles 3: 139-145. (Pubitemid 29250569)
24. Grant WD. (2006). Alkaline environments and biodiversity, in extremophilies. In: Gerday Charles, Glansdorff Nicolas (eds). Encyclopedia of Life Support Systems (EOLSS). Developed under the Auspices of the UNESCO, Eolss Publishers: Oxford, UK. http://www.eolss.net.
25. Grant WD, Heaphy S. (2010). Metagenomics and recovery of enzyme genes from alkaline saline environments. Environ Technol 31: 1135-1143.
26. Grant WD, Sorokin DY. (2011). Distribution and diversity of soda lake alkaliphiles. In: Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO (eds). Extremophiles Handbook vol. 1. Springer: Tokyo, pp. 27-54.
27. Hoeft SE, Kulp TR, Stolz JF, Hollibaugh JT, Oremland RS. (2004). Dissimilatory arsenate reduction with sulfide as electron donor: Experiments with Mono Lake water and isolation of strain MLMS-1, a chemo-autotrophic arsenate-respirer. Appl Env Microb 70: 2741-2747. (Pubitemid 38657787)
28. Hoeft SE, Blum JS, Stolz JF, Tabita FR, Witte B, King GM et al. (2007). Alkalilimnicola ehrlichii sp. nov., a novel, arsenite-oxidizing haloalkaliphilic gammapro-teobacterium capable of chemoautotrophic or hetero-trophic growth with nitrate or oxygen as the electron acceptor. Int J Syst Evol Microbiol 57: 504-512. (Pubitemid 46437862)
29. 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: 1030-1042. (Pubitemid 36204832)
30. Hunger S, Schmidt O, Hilgarth M, Horn MA, Kolb S, Conrad R et al. (2011). Competing formate-and carbon-dioxide utilizing prokaryotes in an anoxic methane-emitting fen soil. Appl Environ Microbiol 77: 3773-3785.
31. Ito S, Kobayashi T, Hatada Y, Horikoshi K. (2005). Enzymes in modern detergents. In: Barredo JL (eds). Microbial Enzymes and Biotransformations. Humana Press: Totowa, NJ, pp. 151-164.
32. Iversen N, Oremland RS, Klug MJ. (1987). Big Soda Lake (Nevada). 3. Pelagic methanogenesis and anaerobic methane oxidation. Limnol Oceanogr 32: 804-814.
33. Jones BE, Grant WD, Duckworth AW, Owenson GG. (1998). Microbial diversity of soda lakes. Extremophiles 2: 191-200. (Pubitemid 28407999)
34. Joshi AA, Kanekar PP, Kelkar AS, Shouche YS, Vani AA, Borgave SB, Sarnaik SS. (2008). Cultivable bacterial diversity of alkaline Lonar Lake, India. Microb Ecol 55: 163-172. (Pubitemid 351171458)
35. 39Ar age of the Lonar crater and consequence for the geochronology of planetary impacts. Geology 39: 671-674.
36. Kaluzhnaya M, Khmelenina V, Eshinimaev B, Suzina N, Nikitin D, Solonin A et al. (2001). Taxonomic characterization of new alkaliphilic and alkalitolerant methanotrophs from soda lakes of the Southeastern Transbaikal region and description of Methylomicro-bium buryatense sp. nov. Syst Appl Microbiol 24: 166-176. (Pubitemid 32705666)
37. Karpeta WP. (1989). Bedded cherts in the Rietgat Formation, Hartbeesfontain, South Africa: a late Archean to early Proterozoic magadiitic alkaline playa lake deposit? South Afr J Geol 92: 29-36.
38. Khmelenina VN, Kalyuzhnaya MG, Starostina NG, Suzina NE, Trotsenko YA. (1997). Isolation and characterization of halotolerant alkaliphilic methanotrophic bacteria from Tuva soda lakes. Curr Microbiol 35: 257-261. (Pubitemid 27494918)
39. Khmelenina VN, Eshinimaev BT, Kalyuzhnaya MG, Trotsenko I. (2000). Potential activity of methane and ammonia oxidation by methanotropic communities from soda lakes of the southern Transbaikal. Mikro-biologiia 69: 553-558.
40. Kovaleva OL, Tourova TP, Muyzer G, Kolganova TV, Sorokin DY. (2011). Diversity of RuBisco and ATP citrate lyase genes in soda lake sediments. FEMS Microbiol Ecol 75: 37-47.
41. Kumar PA, Srinivas TNR, Kumar PP, Madhu S, Shivaji S. (2010a). Nitritalea halalkaliphila gen. nov., sp. nov., an alkaliphilic bacterium of the family 'Cyclobacter-iaceae', phylum Bacteroidetes. Int J Syst Evol Micro-biol 60: 2320-2325.
42. Kumar PA, Srinivas TNR, Madhu S, Manorama R, Shivaji S. (2010b). Indibacter alkaliphilus gen. nov., sp. nov., an alkaliphilic bacterium isolated from a haloalkaline lake. Int J Syst Evol Microbiol 60: 721-726.
43. Kumar PA, Srinivas TNR, Madhu S, Sravan R, Singh S, Naqvi SWA et al. (2012). Cecembia lonarensis gen. nov., sp. nov., a novel haloalkalitolerant bacterium of the family 'Cyclobacteriaceae', isolated from a haloalkaline lake and emended descriptions of the genera Indibacter, Nitritalea and Belliella. Int J Syst Evol Microbiol 62: 2252-2258.
44. LeCleir GR, Buchan A, Maurer J, Moran MA, Hollibaugh JT. (2007). Comparison of chitinolytic enzymes from an alkaline, hypersaline lake and an estuary. Environ Microb 9: 197-205. (Pubitemid 46059010)
45. Lin JL, Radajewski S, Eshinimaev BT, Trotsenko YA, McDonald IR, Murrell JC. (2004). Molecular diversity of methanotrophs in Transbaikal soda lake sediments and identification of potentially active populations by stable isotope probing. Environ Microbiol 6: 1049-1060. (Pubitemid 39275259)
46. Lin JL, Joye SB, Scholten JC, Schafer H, McDonald IR, Murrell JC. (2005). Analysis of methane monooxygen-ase genes in Mono lake suggests that increased methane oxidation activity may correlate with a change in methanotroph community structure. Appl Environ Microbiol 71: 6458-6462. (Pubitemid 41456958)
47. Linhoff BS, Bennett PC, Puntsag T, Gerel O. (2011). Geochemical evolution of uraniferous soda lakes in Eastern Mongolia. Environ Earth Sci 62: 171-183.
48. Maloof AC, Stewart ST, Weiss BP, Soule SA, Swanson-Hysell NL, Louzada KL et al. (2010). Geology of Lonar Crater, India. Geol Soc Am Bull 122: 109-126.
49. McInerney MJ, Bryant MP. (1981). Basic principles of bioconversions in anaerobic digestion and methano-genesis. In: Sofer S, Zaborsky OR (eds). Biomass Conversion Processes for Energy and Fuels. Plenum Press: New York, NY, pp. 277-296.
50. McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM, Schink B et al. (2008). Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. In: Wiegel J, Maier RJ, Adams MWW (eds). Incredible Anaerobes: From Physiology to Genomics to Fuels. New York Academy of Sciences: Boston, MA, pp. 58-72. (Pubitemid 351451151)
51. Melack JM, Kilham P. (1974). Photosynthetic rates of phytoplankton in East African alkaline, saline lakes. Limnol Oceanogr 19: 743-755.
52. Moussard H, Smith TJ, Murrell JC. (2011). DNA-stable isotope probing and gene mining. In: Murrell JC, Whiteley A (eds). Stable Isotope Probing and Related Technologies. ASM press: Washington, DC, 3-24.
53. Neufeld JD, Murrell JC. (2007). Witnessing the last supper of uncultivated microbial cells with Raman-FISH. ISME J 4: 269-270. (Pubitemid 47227848)
54. Oremland RS, Marsh L, Des Marais DJ. (1982). Methano-genesis in Big Soda Lake, Nevada: an alkaline, moderately hypersaline desert lake. Appl Environ Microbiol 43: 462-468.
55. Oremland RS, Cloern JE, Sofer Z, Smith RL, Culbertson CW, Zehr J et al. (1988). Microbial and biogeochemical processes in Big Soda Lake, Nevada. In: Fleet AJ Kelts K, Talbot MR (eds). Lacustrine Petroleum Source Rocks. Geological Society Special Publication: London No.40: pp. 59-75.
56. Oremland RS. (1990). Nitrogen fixation dynamics of two diazotrophic communities in Mono Lake, California. Appl Environ Microbiol 56: 614-622. (Pubitemid 20088428)
57. Oremland RS, Miller LG, Culbertson CW, Robinson S, Smith RL, Lovley DR et al. (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. 704-744.
58. Oremland RS, Stolz JF, Hollibaugh JT. (2004). The microbial arsenic cycle in Mono Lake, California. FEMS Microb Ecol 48: 15-27. (Pubitemid 38393772)
59. Oremland RS, Kulp TR, Switzer Blum J, Hoeft SE, Baesman S, Miller LG, Stolz JF. (2005). A microbial arsenic cycle in a salt saturated, bextreme environment. Science 308: 1305-1308. (Pubitemid 40746125)
60. Pastor JM, Salvador M, Argandona M, Bernal V, Reina-Bueno M, Csonka LN et al. (2010). Ectoines in cell stress protection: uses and biotechnological production. Biotechnol Adv 28: 782-801.
61. Rees HC, Grant WD, Jones BE, Heaphy S. (2004). Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8: 63-71. (Pubitemid 40882703)
62. Sheridan C. (2004). Kenyan dispute illuminates biopros-pecting difficulties. Nat Biotechnol 22: 1337.
63. Sorokin DY. (1998). Occurrence of nitrification in extremely alkaline environments. Microbiology (Moscow, English translation) 67: 335-339. (Pubitemid 128699108)
64. Sorokin DY, Muyzer G, Brinkhoff T, Kuenen JG, Jetten M. (1998). Isolation and characterization of a novel facultatively alkaliphilic Nitrobacter species-Nb. alkalicus. Arch Microbiol 170: 345-352. (Pubitemid 28458132)
65. Sorokin DY, Jones BE, Kuenen JG. (2000a). A novel obligately methylotrophic, methane-oxidizing Methy-lomicrobium species from a highly alkaline environment. Extremophiles 4: 145-155.
66. Sorokin DY, Robertson LA, Kuenen JG. (2000b). Isolation and characterization of obligately chemolithoauto-trophic alkaliphilic sulfur-oxidizing bacteria. Ant V Leeuwenhoek 77: 251-260.
67. Sorokin D, Tourova T, Schmid MC, Wagner M, Koops H, Kuenen JG, Jetten M. (2001). Isolation and properties of obligately chemolithoautotrophic and extremely alkali-tolerant ammonia-oxidizing bacteria from Mongolian soda lakes. Arch Microbiol 176: 170-177. (Pubitemid 32778704)
68. Sorokin DY, Antipov AN, Kuenen JG. (2003). Complete denitrification in coculture of obligately chemo-lithoautotrophic haloalkaliphilic sulfur-oxidizing bacteria from a hypersaline soda lake. Arch Microbiol 180: 127-133. (Pubitemid 36963237)
69. Sorokin DY, Gorlenko VM, Namsaraev BB, Namsaraev ZB, Lysenko AM, Eshinimaev BT et al. (2004). Prokaryotic communities of the north-eastern Mongolian soda lakes. Hydrobiologia 522: 235-248. (Pubitemid 39066899)
70. Sorokin DY, Foti M, Pinkart HC, Muyzer G. (2007). Sulfur-oxidizing bacteria in Soap Lake (Washington, USA), a meromictic, haloalkaline lake with an unprecedented high sulfide content. Appl Environ Microbiol 73: 451-455. (Pubitemid 46147574)
71. Sorokin DY, Kuenen JG, Muyzer G. (2011). The microbial sulfur cycle at extremely haloalkaline conditions of soda lakes. Front Microbiol 2: 44.
72. Srinivas A, Rahul K, Sasikala Ch, Subhash Y, Ramaprasad EV, Ramana ChV. (2012). Georgenia satyanarayanai sp. nov., an alkaliphilic and thermotolerant amylase producing actinobacterium isolated from a soda lake. Int J Syst Evol Microbiol 62: 2405-2409.
73. Surakasi VP, Wani AA, Shouche YS, Ranade DR. (2007). Phylogenetic analysis of methanogenic enrichment cultures obtained from Lonar Lake in India: isolation of Methanocalculus sp. and Methanoculleus sp. Microb Ecol 54: 697-704. (Pubitemid 47624254)
74. Surakasi VP, Antony CP, Sharma S, Patole MS, Shouche YS. (2010). Temporal bacterial diversity and detection of putative methanotrophs in surface mats of Lonar crater lake. J Basic Microbiol 50: 465-474.
75. 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, that respire oxyanions of selenium and arsenic. Arch Microbiol 171: 19-30. (Pubitemid 29142550)
76. Thakker CD, Ranade DR. (2002). Alkalophilic Methano-sarcina isolated from Lonar Lake. Curr Sci 82: 455-458. (Pubitemid 135694134)
77. Trotsenko YA, Khmelenina VN. (2002). Biology of extre-mophilic and extremotolerant methanotrophs. Arch Microbiol 177: 123-131.
78. Wani AA, Surakasi VP, Siddharth J, Raghavan RG, Patole MS, Ranade D, Shouche YS. (2006). Molecular analyses of microbial diversity associated with the Lonar soda lake in India: an impact crater in a basalt area. Res Microbiol 157: 928-937. (Pubitemid 44828464)
79. Ward BB, Martino DP, Diaz MC, Joye SB. (2000). Analysis of ammonia-oxidizing bacteria from a hypersaline Mono Lake, California, on the basis of 16S rRNA sequences. Appl Environ Microbiol 66: 2873-2881. (Pubitemid 30497594)
80. Wüst PK, Horn MA, Drake HL. (2009). Trophic links between fermenters and methanogens in a moderately acidic fen soil. Environ Microbiol 11: 1395-1409.
81. Zavarzin GA, Zhilina TN, Pusheva MA. (1994). Halophilic acetogenic bacteria. In: Drake HL (eds). Acetogenesis. Chapman & Hall: New York, pp 432-444.
82. Zavarzin GA, Zhilina TN, Kevbrin VV. (1999). The alkaliphilic microbial community and its functional diversity. Microbiologiya 68: 503-521. (Pubitemid 129733359)