Microbial Ecology

, 62:399 | Cite as

Culturable Diversity of Heterotrophic Bacteria in Forlidas Pond (Pensacola Mountains) and Lundström Lake (Shackleton Range), Antarctica

  • Karolien Peeters
  • Dominic A. Hodgson
  • Peter Convey
  • Anne WillemsEmail author
Microbiology of Aquatic Systems


Cultivation techniques were used to study the heterotrophic bacterial diversity in two microbial mat samples originating from the littoral zone of two continental Antarctic lakes (Forlidas Pond and Lundström Lake) in the Dufek Massif (within the Pensacola Mountains group of the Transantarctic Mountains) and Shackleton Range, respectively. Nearly 800 isolates were picked after incubation on several growth media at different temperatures. They were grouped using a whole-genome fingerprinting technique, repetitive element palindromic PCR and partial 16S rRNA gene sequencing. Phylogenetic analysis of the complete 16S rRNA gene sequences of 82 representatives showed that the isolates belonged to four major phylogenetic groups: Actinobacteria, Bacteroidetes, Proteobacteria and Firmicutes. A relatively large difference between the samples was apparent. Forlidas Pond is a completely frozen water body underlain by hypersaline brine, with summer thaw forming a slightly saline littoral moat. This was reflected in the bacterial diversity with a dominance of isolates belonging to Firmicutes, whereas isolates from the freshwater Lundström Lake revealed a dominance of Actinobacteria. A total of 42 different genera were recovered, including first records from Antarctica for Albidiferax, Bosea, Curvibacter, Luteimonas, Ornithinibacillus, Pseudoxanthomonas, Sphingopyxis and Spirosoma. Additionally, a considerable number of potential new species and new genera were recovered distributed over different phylogenetic groups. For several species where previously only the type strain was available in cultivation, we report additional strains. Comparison with public databases showed that overall, 72% of the phylotypes are cosmopolitan whereas 23% are currently only known from Antarctica. However, for the Bacteroidetes, the majority of the phylotypes recovered are at present known only from Antarctica and many of these represent previously unknown species.


Actinobacteria Firmicutes Bacteroidetes Brevundimonas Sphingopyxis 
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.



Fieldwork by DAH and PC was supported by the British Antarctic Survey. This study was carried out in the framework of AMBIO, a project funded by the Belgian Science Policy Office (BelSPO) that contributes to IPY research proposal nr. 55 MERGE (Microbiological and Ecological Responses to Global Environmental Changes in Polar Regions). We thank the AMBIO project coordinator Annick Wilmotte. We are grateful to E. Verleyen and K. Van Hoorde for helpful discussion. The study also contributes to the BAS ‘Polar Science for Planet Earth’ and SCAR ‘Evolution and Biodiversity in Antarctica’ programmes.

Supplementary material

248_2011_9842_MOESM1_ESM.pdf (210 kb)
Fig. S1 (PDF 209 kb)
248_2011_9842_MOESM2_ESM.pdf (26 kb)
Fig. S2 (PDF 25 kb)
248_2011_9842_MOESM3_ESM.pdf (25 kb)
Fig. S3 (PDF 24 kb)
248_2011_9842_MOESM4_ESM.pdf (744 kb)
Fig. S4 Phylogenetic tree based on neighbour-joining analysis of the 16S rRNA gene sequence similarities indicating positions of the two phylotypes related to L. rubra. Phylotypes are indicated in bold type. The numbers at branch nodes are bootstrap values shown as percentages of 500 bootstrap replicates (only values >50% are shown). Transfer of L. aurea to the genus Rhodoglobus was recently proposed [4] but not yet validated (PDF 743 kb)
248_2011_9842_MOESM5_ESM.pdf (677 kb)
Fig. S5 Phylogenetic tree based on neighbour-joining analysis of the 16S rRNA gene sequence similarities indicating positions of the two phylotypes related to S. antarctica. Phylotypes are indicated in bold type. The numbers at branch nodes are bootstrap values shown as percentages of 500 bootstrap replicates (only values >50% are shown) (PDF 676 kb)


  1. 1.
    Aislabie JM, Chhour KL, Saul DJ, Miyauchi S, Ayton J, Paetzold RF, Balks MR (2006) Dominant bacteria in soils of Marble Point and Wright Valley, Victoria Land, Antarctica. Soil Biol Biochem 38:3041–3056CrossRefGoogle Scholar
  2. 2.
    Aislabie JM, Jordan S, Barker GM (2008) Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144:9–20CrossRefGoogle Scholar
  3. 3.
    Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169PubMedGoogle Scholar
  4. 4.
    An S-Y, Xiao T, Yokota A (2010) Reclassification of Leifsonia aurea to the genus Rhodoglobus as Rhodoglobus aureus comb. nov., and emended description of Rhodoglobus vestalii Sheridan et al. 2003. J Gen Appl Microbiol 56:53–55PubMedCrossRefGoogle Scholar
  5. 5.
    An SY, Yokota A (2007) The status of the species Leifsonia rubra Reddy et al. 2003. Request for an opinion. Int J Syst Evol Microbiol 57:1163–1163PubMedCrossRefGoogle Scholar
  6. 6.
    Baele M, Vancanneyt M, Devriese LA, Lefebvre K, Swings J, Haesebrouck F (2003) Lactobacillus ingluviei sp. nov., isolated from the intestinal tract of pigeons. Int J Syst Evol Microbiol 53:133–136PubMedCrossRefGoogle Scholar
  7. 7.
    Behrendt JC, Lemasurier WE, Cooper AK, Tessensohn F, Trehu A, Damaske D (1991) Geophysical studies of the West Antarctic rift system. Tectonics 10:1257–1273CrossRefGoogle Scholar
  8. 8.
    Bowman JP, Brown MV, Nichols DS (1997) Biodiversity and ecophysiology of bacteria associated with Antarctic sea ice. Antarct Sci 9:134–142CrossRefGoogle Scholar
  9. 9.
    Bowman JP, McCammon SA, Brown JL, Nichols PD, McMeekin TA (1997) Psychroserpens burtonensis gen. nov., sp. nov., and Gelidibacter algens gen. nov., sp. nov., psychrophilic bacteria isolated from Antarctic lacustrine and sea ice habitats. Int J Syst Bacteriol 47:670–677PubMedCrossRefGoogle Scholar
  10. 10.
    Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 63:3068–3078PubMedGoogle Scholar
  11. 11.
    Bowman JP, Nichols DS (2002) Aequorivita gen. nov., a member of the family Flavobacteriaceae isolated from terrestrial and marine Antarctic habitats. Int J Syst Evol Microbiol 52:1533–1541PubMedCrossRefGoogle Scholar
  12. 12.
    Brambilla E, Hippe H, Hagelstein A, Tindall BJ, Stackebrandt E (2001) 16S rDNA diversity of cultured and uncultured prokaryotes of a mat sample from Lake Fryxell, McMurdo Dry Valleys, Antarctica. Extremophiles 5:23–33PubMedCrossRefGoogle Scholar
  13. 13.
    Bratina BJ, Stevenson BS, Green WJ, Schmidt TM (1998) Manganese reduction by microbes from Oxic regions of the Lake Vanda (Antarctica) water column. Appl Environ Microbiol 64:3791–3797PubMedGoogle Scholar
  14. 14.
    Coenye T, Falsen E, Vancanneyt M, Hoste B, Govan JRW, Kersters K, Vandamme P (1999) Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia gilardii sp. nov. Int J Syst Bacteriol 49:405–413PubMedCrossRefGoogle Scholar
  15. 15.
    Curtis TP, Sloan WT (2004) Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr Opin Microbiol 7:221–226PubMedCrossRefGoogle Scholar
  16. 16.
    Finster KW, Herbert RA, Lomstein BA (2009) Spirosoma spitsbergense sp. nov. and Spirosoma luteum sp. nov., isolated from a high Arctic permafrost soil, and emended description of the genus Spirosoma. Int J Syst Evol Microbiol 59:839–844PubMedCrossRefGoogle Scholar
  17. 17.
    Forsyth G, Logan NA (2000) Isolation of Bacillus thuringiensis from northern Victoria Land, Antarctica. Lett Appl Microbiol 30:263–266PubMedCrossRefGoogle Scholar
  18. 18.
    Franzmann PD, Hopfl P, Weiss N, Tindall BJ (1991) Psychrotrophic, lactic acid-producing bacteria from anoxic waters in Ace Lake, Antarctica—Carnobacterium funditum sp. nov. and Carnobacterium alterfunditum sp. nov. Arch Microbiol 156:255–262PubMedCrossRefGoogle Scholar
  19. 19.
    Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739PubMedCrossRefGoogle Scholar
  20. 20.
    Gevers D, Huys G, Swings J (2001) Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol Lett 205:31–36PubMedCrossRefGoogle Scholar
  21. 21.
    Gonzalez-Toril E, Amils R, Delmas RJ, Petit JR, Komarek J, Elster J (2009) Bacterial diversity of autotrophic enriched cultures from remote, glacial Antarctic, Alpine and Andean aerosol, snow and soil samples. Biogeosciences 6:33–44CrossRefGoogle Scholar
  22. 22.
    Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264Google Scholar
  23. 23.
    Han SK, Nedashkovskaya OI, Mikhailov VV, Kim SB, Bae KS (2003) Salinibacterium amurskyense gen. nov., sp. nov., a novel genus of the family Microbacteriaceae from the marine environment. Int J Syst Evol Microbiol 53:2061–2066PubMedCrossRefGoogle Scholar
  24. 24.
    Hodgson DA, Convey P (2004) Sledge Bravo 2003–2004. BAS Signals in Antarctica of Past Global Changes. Dufek Massif—Pensacola Mountains. Mount Gass—Shackleton Mountains. British Antarctic Survey Scientific Report Ref R/2003/NT1 British Antarctic Survey CambridgeGoogle Scholar
  25. 25.
    Hodgson DA, Convey P, Verleyen E, Vyverman W, McInnes SJ, Sands CJ, Fernández-Carazo R, Wilmotte A, De Wever A, Peeters K, Tavernier I, Willems A (2010) The limnology and biology of the Dufek Massif, Transantarctic Mountains 82° South. Polar Sci 4:197–214CrossRefGoogle Scholar
  26. 26.
    Irgens RL, Gosink JJ, Staley JT (1996) Polaromonas vacuolata gen. nov., sp. nov., a psychrophilic, marine, gas vacuolate bacterium from Antarctica. Int J Syst Bacteriol 46:822–826PubMedCrossRefGoogle Scholar
  27. 27.
    Janda JM, Abbott SL (2002) Bacterial identification for publication: when is enough enough? J Clin Microbiol 40:1887–1891PubMedCrossRefGoogle Scholar
  28. 28.
    Jungblut AD, Allen MA, Burns BP, Neilan BA (2009) Lipid biomarker analysis of cyanobacteria-dominated microbial mats in meltwater ponds on the McMurdo Ice Shelf, Antarctica. Org Geochem 40:258–269CrossRefGoogle Scholar
  29. 29.
    Jungblut AD, Hawes I, Mountfort D, Hitzfeld B, Dietrich DR, Burns BP, Neilan BA (2005) Diversity within cyanobacterial mat communities in variable salinity meltwater ponds of McMurdo Ice Shelf, Antarctica. Environ Microbiol 7:519–529PubMedCrossRefGoogle Scholar
  30. 30.
    Karr EA, Sattley WM, Jung DO, Madigan MT, Achenbach LA (2003) Remarkable diversity of phototrophic purple bacteria in a permanently frozen Antarctic lake. Appl Environ Microbiol 69:4910–4914PubMedCrossRefGoogle Scholar
  31. 31.
    Krishnamurthi S, Bhattacharya A, Mayilraj S, Saha P, Schumann P, Chakrabarti T (2009) Description of Paenisporosarcina quisquiliarum gen. nov., sp. nov., and reclassification of Sporosarcina macmurdoensis Reddy et al. 2003 as Paenisporosarcina macmurdoensis comb. nov. Int J Syst Evol Microbiol 59:1364–1370PubMedCrossRefGoogle Scholar
  32. 32.
    Li HR, Yu Y, Luo W, Zeng YX (2010) Marisediminicola antarctica gen. nov., sp. nov., an actinobacterium isolated from the Antarctic. Int J Syst Evol Microbiol 60:2535–2539PubMedCrossRefGoogle Scholar
  33. 33.
    Logan NA, De Clerck E, Lebbe L, Verhelst A, Goris J, Forsyth G, Rodriguez-Diaz M, Heyndrickx M, De Vos P (2004) Paenibacillus cineris sp. nov. and Paenibacillus cookii sp. nov., from Antarctic volcanic soils and a gelatin-processing plant. Int J Syst Evol Microbiol 54:1071–1076PubMedCrossRefGoogle Scholar
  34. 34.
    Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104:11436–11440PubMedCrossRefGoogle Scholar
  35. 35.
    Magurran AE (1988) Ecological diversity and its measurements. Princeton University Press, New Jersey, p 192Google Scholar
  36. 36.
    Michaud L, Di Cello F, Brilli M, Fani R, Lo Giudice A, Bruni V (2004) Biodiversity of cultivable psychrophilic marine bacteria isolated from Terra Nova Bay (Ross Sea, Antarctica). FEMS Microbiol Lett 230:63–71PubMedCrossRefGoogle Scholar
  37. 37.
    Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70:202–213PubMedCrossRefGoogle Scholar
  38. 38.
    Montes MJ, Bozal N, Mercade E (2008) Marinobacter guineae sp nov., a novel moderately halophilic bacterium from an Antarctic environment. Int J Syst Evol Microbiol 58:1346–1349PubMedCrossRefGoogle Scholar
  39. 39.
    Nedwell DB, Rutter M (1994) Influence of temperature on growth-rate and competition between 2 psychrotolerant Antarctic bacteria—low-temperature diminishes affinity for substrate uptake. Appl Environ Microbiol 60:1984–1992PubMedGoogle Scholar
  40. 40.
    Pearce DA, Bridge PD, Hughes KA, Sattler B, Psenner R, Russell NJ (2009) Microorganisms in the atmosphere over Antarctica. FEMS Microbiol Ecol 69:143–157PubMedCrossRefGoogle Scholar
  41. 41.
    Peeters K, Ertz D, Willems A (2011) Culturable bacterial diversity at the Princess Elisabeth Station (Utsteinen, Sør Rondane Mountains, East Antarctica) harbours many new taxa. Syst Appl Microbiol (in press)Google Scholar
  42. 42.
    Philippot L, Andersson SGE, Battin TJ, Prosser JI, Schimel JP, Whitman WB, Hallin S (2010) The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8:523–529PubMedCrossRefGoogle Scholar
  43. 43.
    Reddy GSN, Aggarwal RK, Matsumoto GI, Shivaji S (2000) Arthrobacter flavus sp. nov., a psychrophilic bacterium isolated from a pond in McMurdo Dry Valley, Antarctica. Int J Syst Evol Microbiol 50:1553–1561PubMedCrossRefGoogle Scholar
  44. 44.
    Reddy GSN, Matsumoto GI, Shivaji S (2003) Sporosarcina macmurdoensis sp. nov., from a cyanobacterial mat sample from a pond in the McMurdo Dry Valleys, Antarctica. Int J Syst Evol Microbiol 53:1363–1367PubMedCrossRefGoogle Scholar
  45. 45.
    Reddy GSN, Prakash JSS, Prabahar V, Matsumoto GI, Stackebrandt E, Shivaji S (2003) Kocuria polaris sp. nov., an orange-pigmented psychrophilic bacterium isolated from an Antarctic cyanobacterial mat sample. Int J Syst Evol Microbiol 53:183–187PubMedCrossRefGoogle Scholar
  46. 46.
    Reddy GSN, Prakash JSS, Srinivas R, Matsumoto GI, Shivaji S (2003) Leifsonia rubra sp. nov. and Leifsonia aurea sp. nov., psychrophiles from a pond in Antarctica. Int J Syst Evol Microbiol 53:977–984PubMedCrossRefGoogle Scholar
  47. 47.
    Reddy GSN, Prakash JSS, Vairamani M, Prabhakar S, Matsumoto GI, Shivaji S (2002) Planococcus antarcticus and Planococcus psychrophilus spp. nov. isolated from cyanobacterial mat samples collected from ponds in Antarctica. Extremophiles 6:253–261PubMedCrossRefGoogle Scholar
  48. 48.
    Roberts D, McMinn A (1996) Relationships between surface sediment diatom assemblages and water chemistry gradients in saline lakes of the Vestfold Hills, Antarctica. Antarct Sci 8:331–341CrossRefGoogle Scholar
  49. 49.
    Saitou N, Nei M (1987) The neighbor joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  50. 50.
    Selbmann L, Zucconi L, Ruisi S, Grube M, Cardinale M, Onofri S (2010) Culturable bacteria associated with Antarctic lichens: affiliation and psychrotolerance. Polar Biol 33:71–83CrossRefGoogle Scholar
  51. 51.
    Sheridan PP, Loveland-Curtze J, Miteva VI, Brenchley JE (2003) Rhodoglobus vestalii gen. nov., sp. nov., a novel psychrophilic organism isolated from an Antarctic Dry Valley lake. Int J Syst Evol Microbiol 53:985–994PubMedCrossRefGoogle Scholar
  52. 52.
    Shivaji S, Reddy GSN, Aduri RP, Kutty R, Ravenschlag K (2004) Bacterial diversity of a soil sample from Schirmacher Oasis, Antarctica. Cell Mol Biol 50:525–536PubMedGoogle Scholar
  53. 53.
    Stach JEM, Maldonado LA, Masson DG, Ward AC, Goodfellow M, Bull AT (2003) Statistical approaches for estimating actinobacterial diversity in marine sediments. Appl Environ Microbiol 69:6189–6200PubMedCrossRefGoogle Scholar
  54. 54.
    Stackebrandt E, Ebers J (2006) Taxonomic parameters revised: tarnished gold standards. Microbiol Today 2006:153–155Google Scholar
  55. 55.
    Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kampfer P, Maiden MCJ, Nesme X, Rossello-Mora R, Swings J, Trueper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047PubMedCrossRefGoogle Scholar
  56. 56.
    Stackebrandt E, Goebel BM (1994) A place for DNA-DNA reassociation and 16S ribosomal RNA sequence analysis in the present species definition in Bacteriology. Int J Syst Bacteriol 44:846–849CrossRefGoogle Scholar
  57. 57.
    Storey BC, Macdonald DIM, Dalziel IWD, Isbell JL, Millar IL (1996) Early Paleozoic sedimentation, magmatism, and deformation in the Pensacola Mountains, Antarctica: the significance of the Ross orogeny. Geol Soc Am Bull 108:685–707CrossRefGoogle Scholar
  58. 58.
    Sutherland DL (2009) Microbial mat communities in response to recent changes in the physiochemical environment of the meltwater ponds on the McMurdo Ice Shelf, Antarctica. Polar Biol 32:1023–1032CrossRefGoogle Scholar
  59. 59.
    Taton A, Grubisic S, Brambilla E, De Wit R, 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 Microbiol 69:5157–5169PubMedCrossRefGoogle Scholar
  60. 60.
    van den Broeke M, van de Berg WJ, van Meijgaard E, Reijmer C (2006) Identification of Antarctic ablation areas using a regional atmospheric climate model. J Geophys Res. doi: 10.1029/2006JD007127 Google Scholar
  61. 61.
    Van Trappen S, Mergaert J, Van Eygen S, Dawyndt P, Cnockaert MC, Swings J (2002) Diversity of 746 heterotrophic bacteria isolated from microbial mats from ten Antarctic lakes. Syst Appl Microbiol 25:603–610PubMedCrossRefGoogle Scholar
  62. 62.
    Vancanneyt M, Mengaud J, Cleenwerck I, Vanhonacker K, Hoste B, Dawyndt P, Degivry MC, Ringuet D, Janssens D, Swings J (2004) Reclassification of Lactobacillus kefirgranum Takizawa et al. 1994 as Lactobacillus kefiranofaciens subsp. kefirgranum subsp. nov. and emended description of L. kefiranofaciens Fujisawa et al. 1988. Int J Syst Evol Microbiol 54:551–556PubMedCrossRefGoogle Scholar
  63. 63.
    Will TM, Zeh A, Gerdes A, Frimmel HE, Millar IL, Schmadicke E (2009) Palaeoproterozoic to Palaeozoic magmatic and metamorphic events in the Shackleton Range, East Antarctica: constraints from zircon and monazite dating, and implications for the amalgamation of Gondwana. Precambrian Res 172:25–45CrossRefGoogle Scholar
  64. 64.
    Yoon JH, Lee KC, Weiss N, Kho YH, Kang KH, Park YH (2001) Sporosarcina aquimarina sp. nov., a bacterium isolated from seawater in Korea, and transfer of Bacillus globisporus (Larkin and Stokes 1967), Bacillus psychrophilus (Nakamura 1984) and Bacillus pasteurii (Chester 1898) to the genus Sporosarcina as Sporosarcina globispora comb. nov., Sporosarcina psychrophila comb. nov. and Sporosarcina pasteurii comb. nov., and emended description of the genus Sporosarcina. Int J Syst Evol Microbiol 51:1079–1086PubMedCrossRefGoogle Scholar
  65. 65.
    Yu Y, Li H, Zeng Y, Chen B (2010) Phylogenetic diversity of culturable bacteria from Antarctic sandy intertidal sediments. Polar Biol 33:869–875CrossRefGoogle Scholar
  66. 66.
    Zdanowski MK, Weglenski P, Golik P, Sasin JM, Borsuk P, Zmuda MJ, Stankovic A (2004) Bacterial diversity in Adelie penguin, Pygoscelis adeliae, guano: molecular and morpho-physiological approaches. FEMS Microbiol Ecol 50:163–173PubMedCrossRefGoogle Scholar
  67. 67.
    Zhang DC, Li HR, Xin YH, Chi ZM, Zhou PJ, Yu Y (2008) Marinobacter psychrophilus sp. nov., a psychrophilic bacterium isolated from the Arctic. Int J Syst Evol Microbiol 58:1463–1466PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Karolien Peeters
    • 1
  • Dominic A. Hodgson
    • 2
  • Peter Convey
    • 2
  • Anne Willems
    • 1
    Email author
  1. 1.Laboratory of Microbiology, Department of Biochemistry and Microbiology, Fac. ScienceGhent UniversityGhentBelgium
  2. 2.British Antarctic Survey, Natural Environment Research Council, High CrossCambridgeUK

Personalised recommendations