Abstract
A range of small- to moderate-scale studies of patterns in bacterial biodiversity have been conducted in Antarctica over the last two decades, most suggesting strong correlations between the described bacterial communities and elements of local environmental heterogeneity. However, very few of these studies have advanced interpretations in terms of spatially associated patterns, despite increasing evidence of patterns in bacterial biogeography globally. This is likely to be a consequence of restricted sampling coverage, with most studies to date focusing only on a few localities within a specific Antarctic region. Clearly, there is now a need for synthesis over a much larger spatial to consolidate the available data. In this study, we collated Antarctic bacterial culture identities based on the 16S rRNA gene information available in the literature and the GenBank database (n > 2,000 sequences). In contrast to some recent evidence for a distinct Antarctic microbiome, our phylogenetic comparisons show that a majority (~75 %) of Antarctic bacterial isolates were highly similar (≥99 % sequence similarity) to those retrieved from tropical and temperate regions, suggesting widespread distribution of eurythermal mesophiles in Antarctic environments. However, across different Antarctic regions, the dominant bacterial genera exhibit some spatially distinct diversity patterns analogous to those recently proposed for Antarctic terrestrial macroorganisms. Taken together, our results highlight the threat of cross-regional homogenisation in Antarctic biodiversity, and the imperative to include microbiota within the framework of biosecurity measures for Antarctica.
Similar content being viewed by others
References
Aislabie J, Foght J, Saul D (2000) Aromatic hydrocarbon-degrading bacteria from soil near Scott Base, Antarctica. Polar Biol 23:183–188
Aislabie J, Saul DJ, Foght JM (2006a) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10:171–179
Aislabie JM, Chhour KL, Saul DJ, Miyauchi S, Ayton J, Paetzold RF, Balks MR (2006b) Dominant bacteria in soils of Marble Point and Wright Valley, Victoria Land, Antarctica. Soil Biol Biochem 38:3041–3056
Aislabie JM, Jordan S, Barker GM (2008) Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144:9–20
Ayub N, Tribelli P, López N (2009) Polyhydroxyalkanoates are essential for maintenance of redox state in the Antarctic bacterium Pseudomonas sp. 14–3 during low temperature adaptation. Extremophiles 13:59–66
Bahl J, Lau MCY, Smith GJD, Vijaykrishna D, Cary SC, Lacap DC, Lee CK, Papke RT, Warren-Rhodes KA, Wong FKY, Mckay CP, Pointing SB (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:1–6
Bakermans C, Ayala-Del-Río HL, Ponder MA, Vishnivetskaya T, Gilichinsky D, Thomashow MF, Tiedje JM (2006) Psychrobacter cryohalolentis sp. nov. and Psychrobacter arcticus sp. nov., isolated from Siberian permafrost. Int J Syst Evolut Microbiol 56:1285–1291
Baraniecki CA, Aislabie J, Foght JM (2002) Characterization of Sphingomonas sp. Ant 17, an aromatic hydrocarbon-degrading bacterium isolated from Antarctic soil. Microb Ecol 43:44–54
Barton LL (2005) Physiological basis for growth in extreme environments. In: Structural and functional relationships in prokaryotes. Springer, New York, pp 348–393
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
Bowman JP, Cavanagh J, Austin JJ, Sanderson K (1996) Novel Psychrobacter species from Antarctic ornithogenic soils. Int J Syst Bacteriol 46:841–848
Bowman JP, Nichols DS, Mcmeekin TA (1997) Psychrobacter glacincola sp. nov, a halotolerant, psychrophilic bacterium isolated from Antarctic sea ice. Syst Appl Microbiol 20:209–215
Bozal N, Montes MJ, Tudela E, Guinea J (2003) Characterization of several Psychrobacter strains isolated from Antarctic environments and description of Psychrobacter luti sp nov and Psychrobacter fozii sp nov. Int J Syst Evolut Microbiol 53:1093–1100
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 5:23–33
Busse HJ, Denner EBM, Buczolits S, Salkinoja-Salonen M, Bennasar A, Kämpfer P (2003) Sphingomonas aurantiaca sp nov., Sphingomonas aerolata sp nov and Sphingomonas faeni sp nov., air- and dustborne and Antarctic, orange-pigmented, psychrotolerant bacteria, and emended description of the genus Sphingomonas. Int J Syst Evolut Microbiol 53:1253–1260
Cary SC, Mcdonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nature Rev Microbiol 8:129–138
Chong CW, Pearce DA, Convey P, Tan GYA, Wong RCS, Tan IKP (2010) High levels of spatial heterogeneity in the biodiversity of soil prokaryotes on Signy Island, Antarctica. Soil Biol Biochem 42:601–610
Chong CW, Pearce D, Convey P, Tan IKP (2012a) The identification of environmental parameters which could influence soil bacterial community composition on the Antarctic Peninsula—a statistical approach. Antarctic Sci 24:249–258
Chong CW, Pearce DA, Convey P, Yew WC, Tan IKP (2012b) Patterns in the distribution of soil bacterial 16S rRNA gene sequences from different regions of Antarctica. Geoderma 181–182:45–55
Chown SL, Convey P (2007) Spatial and temporal variability across life’s hierarchies in the terrestrial Antarctic. Philos Trans R Soc Lond B 362:2307–2331
Chown SL, Convey P (2012) Spatial and temporal variability in terrestrial Antarctic biodiversity. In: Rogers AD, Johnston NM, Murphy EJ, Clarke A (eds) Antarctic ecosystems: An extreme environment in a changing world, 1st edn. Blackwell Publishing Ltd, New York, pp 13–43
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, Mcgarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145
Convey P (2007) Influences on and origins of terrestrial biodiversity of the sub-Antarctic islands. Pap Proc R Soc Tasmania 141:83–93
Convey P (2013) Antarctic Ecosystems. In: Levin SA (ed) Encyclopedia of Biodiversity. Elsevier, San Diego, pp 179–188
Convey P, Stevens MI (2007) Antarctic biodiversity. Science 317:1877–1878
Convey P, JaE Gibson, Hillenbrand CD, Hodgson DA, Pugh PJA, Smellie JL, Stevens MI (2008) Antarctic terrestrial life—challenging the history of the frozen continent? Biol Rev 83:103–117
Convey P, Barnes DKA, Griffiths HJ, Grant SM, Linse K, Thomas DN (2012a) Biogeography and regional classifications of Antarctica. In: Antarctic Ecosystems. Wiley, New York, pp 469-491
Convey P, Hughes KA, Tin T (2012b) Continental governance and environmental management mechanisms under the Antarctic Treaty System: sufficient for the biodiversity challenges of this century? Biodiversity 13:234–248
Cowan DA, Chown SL, Convey P, Tuffin M, Hughes K, Pointing S, Vincent WF (2011a) Non-indigenous microorganisms in the Antarctic: assessing the risks. Trends Microbiol 19:540–548
Cowan D, Pointing S, Stevens M, Craig Cary S, Stomeo F, Tuffin IM (2011b) Distribution and abiotic influences on hypolithic microbial communities in an Antarctic Dry Valley. Polar Biol 34:307–311
de la Torre JR, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69:3858–3867
de Pascale D, de Santi C, Fu J, Landfald B (2012) The microbial diversity of Polar environments is a fertile ground for bioprospecting. Mar Genomics 8:15–22
de Wever A, Leliaert F, Verleyen E, Vanormelingen P, Van Der Gucht K, Hodgson DA, Sabbe K, Vyverman W (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proc R Soc Lond B Bio 276:3591–3599
Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063
Goh YS, Tan IKP (2012) Polyhydroxyalkanoate production by antarctic soil bacteria isolated from Casey Station and Signy Island. Microbiol Res 167:211–219
Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evo 21:501–507
Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654
Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27
Hogg ID, Cary SC, Convey P, Newsham KK, O’Donnell AG, Adams BJ, Aislabie J, Frati F, Stevens MI, Wall DH (2006) Biotic interactions in Antarctic terrestrial ecosystems: are they a factor? Soil Biol Biochem 38:3035–3040
Hughes KA, Convey P (2010) The protection of Antarctic terrestrial ecosystems from inter- and intra-continental transfer of non-indigenous species by human activities: a review of current systems and practices. Global Environ Chang 20:96–112
Hughes KA, Convey P (2012) Determining the native/non-native status of newly discovered terrestrial and freshwater species in Antarctica—current knowledge, methodology and management action. J Environ Manag 93:52–66
Hughes KA, Lawley B (2003) A novel Antarctic microbial endolithic community within gypsum crusts. Environ Microbiol 5:555–565
Hughes KA, Fretwell P, Rae J, Holmes K, Fleming A (2011) Antarctica: mapping a finite and diminishing environmental resource. Antarctic Sci 23:537–548
Hughes KA, Cary CS, Cowan DA, Lovejoy C, Vincent WF, Wilmotte A (2013) Guest editorial: Pristine Antarctica: threats and protection. Antarctic Sci 25:1
Jagannadham MV, Chattopadhyay MK, Subbalakshmi C, Vairamani M, Narayanan K, Rao CM, Shivaji S (2000) Carotenoids of an Antarctic psychrotolerant bacterium, Sphingobacterium antarcticus, and a mesophilic bacterium, Sphingobacterium multivorum. Arch Microbiol 173:418–424
Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728
Kowalchuk GA, Drigo B, Yergeau E, van Veen JA (2006) Assessing bacterial and fungal community structure in soil using ribosomal RNA and other structural gene markers. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer, Berlin, pp 159–188
Lee CK, Barbier BA, Bottos EM, Mcdonald IR, Cary SC (2012) The inter-valley soil comparative survey: the ecology of dry valley edaphic microbial communities. ISME J 6:1046–1057
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371
Ma Y, Wang L, Shao Z (2006) Pseudomonas, the dominant polycyclic aromatic hydrocarbon-degrading bacteria isolated from Antarctic soils and the role of large plasmids in horizontal gene transfer. Environ Microbiol 8:455–465
Magalhães C, Stevens MI, Cary SC, Ball BA, Storey BC, Wall DH, Turk R, Ruprecht U (2012) At limits of life: multidisciplinary insights reveal environmental constraints on biotic diversity in continental Antarctica. PLoS One 7:e44578
Marshall WA (1996) Biological particles over Antarctica. Nature 383:680
Marshall WA, Convey P (1997) Dispersal of moss propagules on Signy Island, maritime Antarctic. Polar Biol 18:376–383
Maruyama A, Honda D, Yamamoto H, Kitamura K, Higashihara T (2000) Phylogenetic analysis of psychrophilic bacteria isolated from the Japan Trench, including a description of the deep-sea species Psychrobacter pacificensis sp. nov. Int J Syst Evolut Microbiol 50:835–846
Michel RFM, Schaefer CEGR, Dias LE, Simas FNB, De Melo Benites V, De Sá Mendonça E (2006) Ornithogenic gelisols (cryosols) from maritime Antarctica. Soil Sci Soc Am J 70:1370–1376
Mikucki JA, Priscu JC (2007) Bacterial diversity associated with Blood Falls, a subglacial outflow from the Taylor Glacier, Antarctica. Appl Environ Microbiol 73:4029–4039
Namsaraev Z, Mano M-J, Fernandez R, Wilmotte A (2010) Biogeography of terrestrial cyanobacteria from Antarctic ice-free areas. Ann Glaciol 51:171–177
Niederberger TD, Mcdonald IR, Hacker AL, Soo RM, Barrett JE, Wall DH, Cary SC (2008) Microbial community composition in soils of Northern Victoria Land, Antarctica. Environ Microbiol 10:1713–1724
Niederberger TD, Perreault NN, Tille S, Lollar BS, Lacrampe-Couloume G, Andersen D, Greer CW, Pollard W, Whyte LG (2010) Microbial characterization of a subzero, hypersaline methane seep in the Canadian High Arctic. ISME J 4:1326–1339
Pearce DA, Van Der Gast CJ, Lawley B, Ellis-Evans JC (2003) Bacterioplankton community diversity in a maritime Antarctic lake, determined by culture-dependent and culture-independent techniques. FEMS Microbiol Ecol 45:59–70
Pearce DA, Bridge PD, Hughes KA, Sattler B, Psenner R, Russell NJ (2009) Microorganisms in the atmosphere over Antarctica. FEMS Microbiol Ecol 69:143–157
Pearce DA, Hughes KA, Lachlan-Cope T, Harangozo SA, Jones AE (2010) Biodiversity of air-borne microorganisms at Halley station, Antarctica. Extremophiles 14:145–159
Pearce DA, Newsham K, Thorne M, Calvo-Bado L, Krsek M, Laskaris P, Hodson A, Wellington EMH (2012) Metagenomic analysis of a southern maritime Antarctic soil. Front Extrem Microbiol 3. doi:10.3389/fmicb.2012.00403
Peat HJ, Clarke A, Convey P (2007) Diversity and biogeography of the Antarctic flora. J Biogeogr 34:132–146
Peeters K, Ertz D, Willems A (2011a) Culturable bacterial diversity at the Princess Elisabeth Station (Utsteinen, Sør Rondane Mountains, East Antarctica) harbours many new taxa. Syst Appl Microbiol 34:360–367
Peeters K, Hodgson D, Convey P, Willems A (2011b) Culturable diversity of heterotrophic bacteria in Forlidas Pond (Pensacola Mountains) and Lundström Lake (Shackleton Range), Antarctica. Microbial Ecol 62:399–413
Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA 106:19964–19969
Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196
Pugh PJA, Convey P (2008) Surviving out in the cold: Antarctic endemic invertebrates and their refugia. J Biogeogr 35:2176–2186
Reddy GSN, Prakash JSS, Matsumoto GI, Stackebrandt E, Shivaji S (2002) Arthrobacter roseus sp nov., a psychrophilic bacterium isolated from an Antarctic cyanobacterial mat sample. Int J Syst Evolut Microbiol 52:1017–1021
Rodrigues DF, Da CJE, Ayala-Del-Rio HL, Pellizari VH, Gilichinsky D, Sepulveda-Torres L, Tiedje JM (2009) Biogeography of two cold-adapted genera: Psychrobacter and Exiguobacterium. ISME J 3:658–665
Rojas JL, Martin J, Tormo JR, Vicente F, Brunati M, Ciciliato I, Losi D, Van Trappen S, Mergaert J, Swings J, Marinelli F, Genilloud O (2009) Bacterial diversity from benthic mats of Antarctic lakes as a source of new bioactive metabolites. Mar Genomics 2:33–41
Saul DJ, Aislabie JM, Brown CE, Harris L, Foght JM (2005) Hydrocarbon contamination changes the bacterial diversity of soil from around Scott Base, Antarctica. FEMS Microbiol Ecol 53:141–155
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Selkirk PM (2007) The nature and importance of the sub-Antarctic. Pap Proc R Soc Tasmania 141:1–6
Shivaji S, Pratibha MS, Sailaja B, Hara Kishore K, Singh AK, Begum Z, Anarasi U, Prabagaran SR, Reddy GS, Srinivas TN (2011) Bacterial diversity of soil in the vicinity of Pindari glacier, Himalayan mountain ranges, India, using culturable bacteria and soil 16S rRNA gene clones. Extremophiles 15:1–22
Shravage BV, Dayananda KM, Patole MS, Shouche YS (2007) Molecular microbial diversity of a soil sample and detection of ammonia oxidizers from Cape Evans, Mcmurdo Dry Valley, Antarctica. Microbiol Res 162:15–25
Smith RIL (1984) Terrestrial plant biology of the subantarctic and Antarctic. In: Laws RM (ed) Antarctic Ecology. Academic Press, London, pp 61–162
Staley JT, Gosink JJ (1999) Poles apart: biodiversity and biogeography of sea ice bacteria. Ann Rev Microbiol 53:189–215
Stingl U, Cho JC, Foo W, Vergin KL, Lanoil B, Giovannoni SJ (2008) Dilution-to-extinction culturing of psychrotolerant planktonic bacteria from permanently ice-covered lakes in the McMurdo Dry Valleys, Antarctica. Microb Ecol 55:395–405
Stomeo F, Makhalanyane TP, Valverde A, Pointing SB, Stevens MI, Cary CS, Tuffin MI, Cowan DA (2012) Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated Antarctic Dry Valley. FEMS Microbiol Ecol 82:326–340
Taton A, Grubisic S, Balthasart P, Hodgson DA, Laybourn-Parry J, Wilmotte A (2006) Biogeographical distribution and ecological ranges of benthic cyanobacteria in East Antarctic lakes. FEMS Microbiol Ecol 57:272–289
Tayeb LA, Lefevre M, Passet V, Diancourt L, Brisse S, PaD Grimont (2008) Comparative phylogenies of Burkholderia, Ralstonia, Comamonas, Brevundimonas and related organisms derived from rpoB, gyrB and rrs gene sequences. Res Microbiol 159:169–177
Terauds A, Chown SL, Morgan F, Peat HJ, Watts DJ, Keys H, Convey P, Bergstrom DM (2012) Conservation biogeography of the Antarctic. Divers Distrib 18:726–741
Tin T, Fleming ZL, Hughes KA, Ainley DG, Convey P, Moreno CA, Pfeiffer S, Scott J, Snape I (2009) Impacts of local human activities on the Antarctic environment. Antarctic Sci 21:3–33
Tindall BJ (2004) Prokaryotic diversity in the Antarctic: the tip of the iceberg. Microbial Ecol 47:271–283
Van Trappen S (2009) Diversity of Flavobacterium spp. in polar aquatic environments. In: Second conference on members of the genus Flavobacterium Paris. Institut National de la Recherche Agronomique (INRA), France
Van Trappen S, Vandecandelaere I, Mergaert J, Swings J (2004) Flavobacterium degerlachei sp nov., Flavobacterium frigoris sp nov and Flavobacterium micromati sp nov., novel psychrophilic bacteria isolated from microbial mats in Antarctic lakes. Int J Syst Evolut Microbiol 54:85–92
Vincent WF (2000) Evolutionary origins of Antarctic microbiota: invasion, selection and endemism. Antarctic Sci 12:374–385
Vyverman W, Verleyen E, Wilmotte A, Hodgson DA, Willems A, Peeters K, Van De Vijver B, De Wever A, Leliaert F, Sabbe K (2010) Evidence for widespread endemism among Antarctic micro-organisms. Polar Sci 4:103–113
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Winsley T, Van Dorst J, Brown M, Ferrari B (2012) Capturing greater 16S rRNA gene sequence diversity within the domain bacteria. Appl Environ Microbiol 78:5938–5941
Yergeau E, Bokhorst S, Huiskes AHL, Boschker HTS, Aerts R, Kowalchuk GA (2007a) Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. FEMS Microbiol Ecol 59:436–451
Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007b) Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ Microbiol 9:2670–2682
Yi H, Oh HM, Lee JH, Kim SJ, Chun J (2005) Flavobacterium antarcticum sp. nov., a novel psychrotolerant bacterium isolated from the Antarctic. Int J Syst Evolut Microbiol 55:637–641
Zdanowski MK, Zmuda MJ, Zwolska I (2005) Bacterial role in the decomposition of marine-derived material (penguin guano) in the terrestrial maritime Antarctic. Soil Biol Biochem 37:581–595
Acknowledgments
This study was supported by University of Malaya (UM) Research Grant RG020/09SUS, and partially supported by UM Postdoctoral Fellowship to Chong Chun Wie. We thank Peter Fretwell (BAS Mapping and Geographic Information Centre) for Fig. 2, and Prof. Aharon Oren and an anonymous reviewer for their constructive comments and suggestions on an earlier version of this paper. This paper contributes to the BAS ‘Polar Science for Planet Earth’ and SCAR ‘Evolution and Biodiversity in Antarctica’ research programmes.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Oren.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chong, C.W., Goh, Y.S., Convey, P. et al. Spatial pattern in Antarctica: what can we learn from Antarctic bacterial isolates?. Extremophiles 17, 733–745 (2013). https://doi.org/10.1007/s00792-013-0555-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-013-0555-3