Abstract
Polar Regions (continental Antarctica and the Arctic) are characterized by a range of extreme environmental conditions, which impose severe pressures on biological life. Polar cold-active cyanobacteria are uniquely adapted to withstand the environmental conditions of the high latitudes. These adaptations include high ultra-violet radiation and desiccation tolerance, and mechanisms to protect cells from freeze–thaw damage. As the most widely distributed photoautotrophs in these regions, cyanobacteria are likely the dominant contributors of critically essential ecosystem services, particularly carbon and nitrogen turnover in terrestrial polar habitats. These habitats include soils, permafrost, cryptic niches (including biological soil crusts, hypoliths and endoliths), ice and snow, and a range of aquatic habitats. Here we review current literature on the ecology, and the functional role played by cyanobacteria in various Arctic and Antarctic environments. We focus on the ecological importance of cyanobacterial communities in Polar Regions and assess what is known regarding the toxins they produce. We also review the responses and adaptations of cyanobacteria to extreme environments.
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References
Adriaenssens EM, Guerrero LD, Makhalanyan TP, Aislabie JM, Cowan DA (2014) Draft genome sequence of the aromatic hydrocarbon-degrading bacterium Sphingobium sp. Strain Ant17, isolated from Antarctic soil. Genom Announc. doi:10.1128/genomeA.00212-14
Agawin NS, Agusti S (1997) Abundance, frequency of dividing cells and growth rates of Synechococcus sp. (cyanobacteria) in the stratified Northwest Mediterranean Sea. J Plankton Res 19:1599–1615
Aislabie JM, Chhour K-L, 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 38:3041–3056. doi:10.1016/j.soilbio.2006.02.018
Aislabie J, Jordan S, Barker G (2008) Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144:9–20
Babalola OO, Kirby BM, Le Roes-Hill M, Cook AE, Cary SC, Burton SG, Cowan DA (2009) Phylogenetic analysis of actinobacterial populations associated with Antarctic Dry Valley mineral soils. Environ Microbiol 11:566–576. doi:10.1111/j.1462-2920.2008.01809.x
Bahl J et al (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:163. doi:10.1038/ncomms1167
Bakermans C, Skidmore ML, Douglas S, McKay CP (2014) Molecular characterization of bacteria from permafrost of the Taylor Valley, Antarctica. FEMS Microbiol Ecol 89(2):331–346
Belnap J (2003) The world at your feet: desert biological soil crusts. Front Ecol Environ 1:181–189
Belnap J, Gardner JS (1993) Soil microstructure in soils of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus. West N Am Nat 53:40–47
Belnap J, Lange OL (2002) Biological soil crusts: structure, function, and management; with 30 tables, vol 150. Springer, Berlin
Benhua S et al (2014) Biogeochemical responses to nutrient, moisture and temperature manipulations of soil from Signy Island, South Orkney Islands in the Maritime Antarctic. Antarct Sci 26(5):513–520
Blanco Y et al (2012) Prokaryotic communities and operating metabolisms in the surface and the permafrost of Deception Island (Antarctica). Environ Microbiol 14:2495–2510. doi:10.1111/j.1462-2920.2012.02767.x
Bockheim JG, McLeod M (2008) Soil distribution in the McMurdo Dry Valleys, Antarctica. Geoderma 144:43–49
Bonilla S, Villeneuve V, Vincent WF (2005) Benthic and planktonic algal communities in a high arctic lake: pigment structure and contrasting responses to nutrient enrichment. J Phycol 41:1120–1130
Bottos EM, Vincent WF, Greer CW, Whyte LG (2008) Prokaryotic diversity of arctic ice shelf microbial mats. Environ Microbiol 10:950–966
Bowker MA, Maestre FT, Eldridge D, Belnap J, Castillo-Monroy A, Escolar C, Soliveres S (2014) Biological soil crusts (biocrusts) as a model system in community, landscape and ecosystem ecology. Biodivers Conserv 23:1619–1637
Büdel B, Colesie C (2014) Biological soil crusts. Antarctic terrestrial microbiology. Springer, Berlin, pp 131–161
Büdel B, Bendix J, Bicker FR, Allan Green T (2008) Dewfall as a water source frequently activates the endolithic cyanobacterial communities in the granites of Taylor Valley, Antarctica. J Phycol 44:1415–1424
Büdel B et al (2014) Improved appreciation of the functioning and importance of biological soil crusts in Europe: the Soil Crust International Project (SCIN). Biodivers Conserv 23(7):1619–1637
Büdel B, Schulz B, Reichenberger H, Bicker F, Green T (2009) Cryptoendolithic cyanobacteria from calcite marble rock ridges, Taylor Valley, Antarctica. Algol Stud 129:61–69
Busch A, Friedrich B, Cramm R (2002) Characterization of the norB gene, encoding nitric oxide reductase, in the nondenitrifying cyanobacterium Synechocystis sp. strain PCC6803. Appl Environ Microbiol 68:668–672
Cameron KA, Hodson AJ, Osborn AM (2012) Structure and diversity of bacterial, eukaryotic and archaeal communities in glacial cryoconite holes from the Arctic and the Antarctic. FEMS Microbiol Ecol 82:254–267. doi:10.1111/j.1574-6941.2011.01277.x
Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8:129–138. doi:10.1038/nrmicro2281
Castenholz RW (1988) Culturing methods for cyanobacteria. Methods Enzymol 167:68–93
Castillo-Monroy AP, Maestre FT, Delgado-Baquerizo M, Gallardo A (2010) Biological soil crusts modulate nitrogen availability in semi-arid ecosystems: insights from a Mediterranean grassland. Plant Soil 333:21–34
Krembs C, Eicken H, Junge K, Deming J (2002) High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep Sea Res Part I 49:2163–2181
Chan Y et al (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14:2272–2282. doi:10.1111/j.1462-2920.2012.02821.x
Chan Y, Van Nostrand JD, Zhou J, Pointing SB, Farrell RL (2013) Functional ecology of an Antarctic Dry Valley. Proc Natl Acad Sci. doi:10.1073/pnas.1300643110
Cockell CS, Stokes MD (2004) Ecology: widespread colonization by polar hypoliths. Nature 431:414–414. http://www.nature.com/nature/journal/v431/n7007/suppinfo/431414a_S1.html
Cockell C, Rettberg P, Horneck G, Scherer K, Stokes DM (2003) Measurements of microbial protection from ultraviolet radiation in polar terrestrial microhabitats. Polar Biol 26:62–69
Convey P et al (2014) The spatial structure of Antarctic biodiversity. Ecol Monogr 84:203–244. doi:10.1890/12-2216.1
Cowan DA, Ah Tow LA (2004) Endangered antarctic environments. Annu Rev Microbiol 58:649–690. doi:10.1146/annurev.micro.57.030502.090811
Cowan DA, Khan N, Pointing SB, Cary SC (2010) Diverse hypolithic refuge communities in the McMurdo Dry Valleys. Antarct Sci 22:714–720. doi:10.1017/s0954102010000507
Cowan DA, Sohm JA, Makhalanyane TP, Capone DG, Green TGA, Cary SC, Tuffin IM (2011) Hypolithic communities: important nitrogen sources in Antarctic desert soils. Environ Microbiol Rep 3:581–586. doi:10.1111/j.1758-2229.2011.00266.x
Cowan DA, Makhalanyane TP, Dennis PG, Hopkins DW (2014) Microbial ecology and biogeochemistry of continental Antarctic soils. Front Microbiol 5:154. doi:10.3389/fmicb.2014.00154
Curtis T (2006) Microbial ecologists: it’s time to’go large’. Nat Rev Microbiol 4:488
D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389
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. doi:10.1128/aem.69.7.3858-3867.2003
de los Rios A, Wierzchos J, Sancho LG, Ascaso C (2004) Exploring the physiological state of continental Antarctic endolithic microorganisms by microscopy. FEMS Microbiol Ecol 50:143–152. doi:10.1016/j.femsec.2004.06.010
de los Rios A, Sancho LG, Grube M, Wierzchos J, Ascaso C (2005) Endolithic growth of two Lecidea lichens in granite from continental Antarctica detected by molecular and microscopy techniques. New Phytol 165:181–190
de los Rios A, Cary C, Cowan D (2014) The spatial structures of hypolithic communities in the Dry Valleys of East Antarctica. Polar Biol. doi:10.1007/s00300-014-1564-0
Dennis PG, Newsham KK, Rushton SP, Ord VJ, O’Donnell AG, Hopkins DW (2013) Warming constrains bacterial community responses to nutrient inputs in a southern, but not northern, maritime Antarctic soil. Soil Biol Biochem 57:248–255. doi:10.1016/j.soilbio.2012.07.009
Dupraz C, Reid RP, Braissant O, Decho AW, Norman RS, Visscher PT (2009) Processes of carbonate precipitation in modern microbial mats. Earth-Sci Rev 96:141–162
Edwards A et al (2011) Possible interactions between bacterial diversity, microbial activity and supraglacial hydrology of cryoconite holes in Svalbard. ISME J 5:150–160. doi:10.1038/ismej.2010.100
Escolar C, Martínez I, Bowker MA, Maestre FT (2012) Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning. Philos Trans R Soc B 367:3087–3099
Evans SE, Wallenstein MD (2014) Climate change alters ecological strategies of soil bacteria. Ecol Lett 17:155–164. doi:10.1111/ele.12206
Fernández A, Mouriño-Carballido B, Bode A, Varela M, Marañón E (2010) Latitudinal distribution of Trichodesmium spp. and N2 fixation in the Atlantic Ocean. Biogeosci Discuss 7:2195–2225
Fernández-Valiente E, Quesada A, Howard-Williams C, Hawes I (2001) N2-fixation in cyanobacterial mats from ponds on the McMurdo Ice Shelf, Antarctica. Microb Ecol 42:338–349
Ferreras ER, De Maayer P, Makhalanyane TP, Guerrero LD, Aislabie JM, Cowan DA (2014) Draft genome sequence of Microbacterium sp. strain CH12i, isolated from shallow groundwater in Cape Hallett, Antarctica. Genom Announc 2:e00789
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631. doi:10.1073/pnas.0507535103
Fierer N, Schimel JP, Holden PA (2003) Influence of drying-rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71. doi:10.1007/s00248-002-1007-2
Foreman CM, Sattler B, Mikucki JA, Porazinska DL, Priscu JC (2007) Metabolic activity and diversity of cryoconites in the Taylor Valley. Antarct J Geophys Res 2005–2012:112
Frank-Fahle BA, Yergeau É, Greer CW, Lantuit H, Wagner D (2014) Microbial functional potential and community composition in permafrost-affected soils of the NW Canadian Arctic. PLoS One 9:e84761
Friedmann EI, Hua M, Ocampo-Friedmann R (1988) Cryptoendolithic lichen and cyanobacterial communities of the Ross Desert. Antarct Polarforschung 58:251–259
Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317
Garcia-Pichel F, Pringault O (2001) Microbiology—Cyanobacteria track water in desert soils. Nature 413:380–381. doi:10.1038/35096640
Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka RM (2013) Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340:1574–1577
Gilichinsky D et al (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age, and implication for astrobiology. Astrobiology 7:275–311
Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Res 51:475–478
Guerrero LD, Makhalanyane TP, Aislabie JM, Cowan DA (2014) Draft Genome Sequence of Williamsia sp. Strain D3, Isolated From the Darwin Mountains, Antarctica. Genom Announc doi:10.1128/genomeA.01230-13
Harding T, Jungblut AD, Lovejoy C, Vincent WF (2011) Microbes in high arctic snow and implications for the cold biosphere. Appl Environ Microbiol 77:3234–3243. doi:10.1128/AEM.02611-10
Hopkins DW et al (2008) Enzymatic activities and microbial communities in an Antarctic dry valley soil: Responses to C and N supplementation. Soil Biol Biochem 40:2130–2136. doi:10.1016/j.soilbio.2008.03.022
Hopkins DW et al (2009) Isotopic evidence for the provenance and turnover of organic carbon by soil microorganisms in the Antarctic dry valleys. Environ Microbiol 11:597–608. doi:10.1111/j.1462-2920.2008.01830.x
Hopkins D, Newsham K, Dungait J (2014) Primary production and links to carbon cycling in Antarctic soils. Antarctic Terrestrial Microbiology. Springer, Berlin, pp 233–248
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton
Hughes KA, Lawley B (2003) A novel Antarctic microbial endolithic community within gypsum crusts. Environ Microbiol 5:555–565
Jansson JK, Taş N (2014) The microbial ecology of permafrost. Nat Rev Microbiol 6:414–425
Jochimsen EM et al (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N Engl J Med 338:873–878
Johnson-Rollings AS et al (2014) Exploring the functional soil-microbe interface and exoenzymes through soil metaexoproteomics. ISME J. doi:10.1038/ismej.2014.130
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 7:519–529. doi:10.1111/j.1462-2920.2005.00717.x
Jungblut AD, Lovejoy C, Vincent WF (2010) Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J 4:191–202. doi:10.1038/ismej.2009.113
Jungblut AD, Wood SA, Hawes I, Webster-Brown J, Harris C (2012) The Pyramid Trough Wetland: environmental and biological diversity in a newly created Antarctic protected area. FEMS Microbiol Ecol 82:356–366
Kaštovská K, Elster J, Stibal M, Šantrůčková H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (High Arctic). Microb Ecol 50:396–407
Khan N, Tuffin M, Stafford W, Cary C, Lacap DC, Pointing SB, Cowan D (2011) Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biol 34:1657–1668. doi:10.1007/s00300-011-1061-7
Kimble J (2004) Cryosols: permafrost-affected soils. Springer Science, Berlin
Kleinteich J, Wood SA, Küpper FC, Camacho A, Quesada A, Frickey T, Dietrich DR (2012) Temperature-related changes in polar cyanobacterial mat diversity and toxin production Nature. Clim Change 2:356–360
Kleinteich J et al (2014) Diversity of toxin and non-toxin containing cyanobacterial mats of meltwater ponds on the Antarctic Peninsula: a pyrosequencing approach. Antarct Sci FirstView. doi:10.1017/S0954102014000145
Koch C (2012) Modular biological complexity. Science 337:531–532
Komárek O, Komárek J (2010) Diversity and Ecology of Cyanobacterial Microflora of Antarctic Seepage Habitats: comparison of King George Island, Shetland Islands, and James Ross Island, NW Weddell Sea, Antarctica. Microbial Mats. Springer, Berlin, pp 515–539
Komárek J, Elster J, Komárek O (2008) Diversity of the cyanobacterial microflora of the northern part of James Ross Island, NW Weddell Sea, Antarctica. Polar Biol 31:853–865
Larson CA, Passy SI (2013) Rates of species accumulation and taxonomic diversification during phototrophic biofilm development are controlled by both nutrient supply and current velocity. Appl Environ Microbiol 79:2054–2060
Lauro FM et al (2010) An integrative study of a meromictic lake ecosystem in Antarctica. Isme J 5:879–895
Laybourn-Parry J, Bell EM (2014) Ace Lake: three decades of research on a meromictic, Antarctic lake. Polar Biol 37:1685–1699
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. doi:10.1038/ismej.2011.170
Ling HU, Seppelt RD (1998) Non-marine algae and cyanobacteria of the Windmill Islands region, Antarctica with descriptions of two new species. Archiv für Hydrobiol 124:49–62
Lizotte MP (2008) Phytoplankton and primary production Polar lakes and rivers. Oxford University Press, Oxford, pp 157–178
Los D, Mironov K (2013) Membrane properties and cold stress responses in cyanobacteria and plants. FEBS Journal. Wiley, Hoboken, p 224
Lyons WB, Leslie DL, Harmon RS, Neumann K, Welch KA, Bisson KM, McKnight DM (2013) The carbon stable isotope biogeochemistry of streams, Taylor Valley, Antarctica. Appl Geochem 32:26–36. doi:10.1016/j.apgeochem.2012.08.019
Maestre FT et al (2013) Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Global Change Biol 19:3835–3847
Makhalanyane TP, Valverde A, Birkeland N-K, Cary SC, Marla Tuffin I, Cowan DA (2013a) Evidence for successional development in Antarctic hypolithic bacterial communities. Isme J 7:2080–2090. doi:10.1038/ismej.2013.94
Makhalanyane TP, Valverde A, Lacap DC, Pointing SB, Tuffin MI, Cowan DA (2013b) Evidence of species recruitment and development of hot desert hypolithic communities. Environ Microbiol Rep 5:219–224. doi:10.1111/1758-2229.12003
Makhalanyane TP, Pointing SB, Cowan DA (2014) Lithobionts: cryptic and refuge niches. In: Cowan DA (ed) Antarctic terrestrial microbiology: physical and biological properties of Antarctic soils. Springer, Berlin, pp 163–179
Makhalanyane TP, Valverde A, Gunnigle E, Frossard A, Ramond JB, Cowan DA (2015) Microbial ecology of hot desert edaphic systems. FEMS Microbiol Rev. doi:10.1093/femsre/fuu011
Moreira C, Ramos V, Azevedo J, Vasconcelos V (2014) Methods to detect cyanobacteria and their toxins in the environment. Appl Microbiol Biotechnol 98:8073–8082
Mosier AC, Li Z, Thomas BC, Hettich RL, Pan C, Banfield JF (2014) Elevated temperature alters proteomic responses of individual organisms within a biofilm community. ISME J. doi:10.1038/ismej.2014.113
Mueller DR, Vincent WF, Pollard WH, Fritsen CH (2001) Glacial cryoconite ecosystems: a bipolar comparison of algal communities and habitats. Nova Hedwigia Beiheft 123:173–198
Nadeau TL, Castenholz RW (2000) Characterization of psychrophilic oscillatorians (cyanobacteria) from Antarctic meltwater ponds. J Phycol 36:914–923
Namsaraev Z, Mano M-J, Fernandez R, Wilmotte A (2010) Biogeography of terrestrial cyanobacteria from Antarctic ice-free areas. Ann Glaciol 51:171–177
Neilan BA, Pearson LA, Muenchhoff J, Moffitt MC, Dittmann E (2013) Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ Microbiol 15:1239–1253
Ng C et al (2010) Metaproteogenomic analysis of a dominant green sulfur bacterium from Ace Lake. Antarctica Isme J 4:1002–1019. doi:10.1038/ismej.2010.28
Nichols CA, Guezennec J, Bowman JP (2005) Bacterial exopolysaccharides from extreme marine environments with special consideration of the southern ocean, sea ice, and deep-sea hydrothermal vents: a review. Mar Biotechnol (NY) 7:253–271. doi:10.1007/s10126-004-5118-2
Niederberger TD, Sohm JA, Tirindelli J, Gunderson T, Capone DG, Carpenter EJ, Cary SC (2012) Diverse and highly active diazotrophic assemblages inhabit ephemerally wetted soils of the Antarctic Dry Valleys. FEMS Microbiol Ecol 82:376–390. doi:10.1111/j.1574-6941.2012.01390.x
Nienow J, Friedmann E, Ocampo-Friedmann R (2003) Endolithic microorganisms in arid regions. In: Bitton G (ed) Encyclopedia of environmental microbiology. Wiley, New York
Novis PM et al (2007) Annual carbon fixation in terrestrial populations of Nostoc commune (Cyanobacteria) from an Antarctic dry valley is driven by temperature regime. Global Change Biol 13:1224–1237
Oppenheim DR, Paterson DM (1990) The fine structure of an algal mat from a freshwater maritime Antarctic lake. Can J Bot 68:174–183
Oren A (2011) Cyanobacterial systematics and nomenclature as featured in the international bulletin of bacteriological nomenclature and taxonomy/international journal of systematic bacteriology/international journal of systematic and evolutionary microbiology. Int J Syst Evol Microbiol 61:10–15
Oren A (2014) Cyanobacteria: biology, ecology and evolution cyanobacteria: an economic perspective. Bioinformatics 20:1453–1454
Otero X, Fernandez S, de Pablo Hernandez M, Nizoli E, Quesada A (2013) Plant communities as a key factor in biogeochemical processes involving micronutrients (Fe, Mn Co, and Cu) in Antarctic soils (Byers Peninsula, maritime Antarctica). Geoderma 195:145–154
Paerl H, Pinckney J (1996) A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microb Ecol 31:225–247
Pankow H, Haendel D, Richter W (1991) Die Algenflora der Schirmacheroase (Ostantarktika) Beihefte zur. Nova Hedwigia 103:1–195
Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5:650–659
Pearce DA et al (2012) Metagenomic analysis of a southern maritime Antarctic soil. Front Microbiol. doi:10.3389/fmicb.2012.00403
Petroff AP, Sim MS, Maslov A, Krupenin M, Rothman DH, Bosak T (2010) Biophysical basis for the geometry of conical stromatolites. Proc Natl Acad Sci USA 107:9956–9961
Philippot L et al (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619. doi:10.1038/ismej.2013.34
Pinnaka AK, Singh A, Ara S, Begum Z, Reddy GS, Shivaji S (2013) Draft genome sequence of Leifsonia rubra strain CMS 76RT, isolated from a cyanobacterial mat sample from a pond in Wright Valley, McMurdo, Antarctica. Genom Announc. doi:10.1128/genomeA.00633-13
Podgorny IA, Grenfell TC (1996) Absorption of solar energy in a cryoconite hole. Geophys Res Lett 23:2465–2468
Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562. doi:10.1038/nrmicro2831
Pointing SB, Belnap J (2014) Disturbance to desert soil ecosystems contributes to dust-mediated impacts at regional scales. Biodivers Conserv 23:1659–1667
Pointing SB, Chan Y, Lacap DC, Lau MC, Jurgens JA, Farrell RL (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA 106:19964–19969. doi:10.1073/pnas.0908274106
Powell L, Bowman J, Skerratt J, Franzmann P, Burton H (2005) Ecology of a novel Synechococcus clade occurring in dense populations in saline Antarctic lakes. Mar Ecol Prog Ser 291:65–80
Quiblier C, Wood S, Echenique-Subiabre I, Heath M, Villeneuve A, Humbert J-F (2013) A review of current knowledge on toxic benthic freshwater cyanobacteria—ecology, toxin production and risk management. Water Res 47:5464–5479. doi:10.1016/j.watres.2013.06.042
Rae BD, Long BM, Badger MR, Price GD (2013) Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in cyanobacteria and some proteobacteria. Microbiol Mol Biol Rev 77:357–379
Ramond JB, Makhalanyane TP, Tuffin MI, Cowan DA (2015) Normalization of environmental metagenomic DNA enhances the discovery of under-represented microbial community members. Lett Appl Microbiol. doi:10.1111/lam.12380
Reddy GS, Ara S, Singh A, Kumar Pinnaka A, Shivaji S (2013) Draft genome sequence of Psychrobacter aquaticus Strain CMS 56T, isolated from a cyanobacterial Mat Sample collected from water bodies in the McMurdo Dry Valley Region of Antarctica. Genom Announc. doi:10.1128/genomeA.00918-13
Rocak S, Linder P (2004) DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 5:232–241
Rochera C, Villaescusa JA, Velázquez D, Fernández-Valiente E, Quesada A, Camacho A (2013) Vertical structure of bi-layered microbial mats from Byers Peninsula, Maritime Antarctica. Antarct Sci 25:270–276
Ronca S, Frossard A, Guerrero LD, Makhalanyane TP, Aislabie JM, Cowan DA (2015) Draft genome sequence of Sphingomonas sp. strain Ant20, isolated from oil-contaminated soil on Ross Island, Antarctica. Genom Announc 3:e01309–e01314
Sabbe K, Hodgson DA, Verleyen E, Taton A, Wilmotte A, Vanhoutte K, Vyverman W (2004) Salinity, depth and the structure and composition of microbial mats in continental Antarctic lakes. Freshwater Biol 49:296–319
Santos HF et al (2014) Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J. doi:10.1038/ismej.2014.70
Schlesinger WH, Pippen JS, Wallenstein MD, Hofmockel KS, Klepeis DM, Mahall BE (2003) Community composition and photosynthesis by photoautotrophs under quartz pebbles, Southern Mojave Desert. Ecology 84:3222–3231. doi:10.1890/02-0549
Seckbach J, Oren A (2010) Microbial mats: modern and ancient microorganisms in stratified systems, vol 14. Springer, Berlin
Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790
Singh BK et al (2014) Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environ Microbiol. doi:10.1111/1462-2920.12353
Smith MC, Bowman JP, Scott FJ, Line MA (2000) Sublithic bacteria associated with Antarctic quartz stones. Antarct Sci 12:177–184
Stanish LF et al (2013) Bacteria and diatom co-occurrence patterns in microbial mats from polar desert streams. Environ Microbiol 15:1115–1131
Steig EJ, Orsi AJ (2013) Climate science: the heat is on in Antarctica. Nat Geosci 6:87–88
Steven B, Pollard WH, Greer CW, Whyte LG (2008) Microbial diversity and activity through a permafrost/ground ice core profile from the Canadian high Arctic. Environ Microbiol 10:3388–3403
Steven B, Gallegos-Graves LV, Belnap J, Kuske CR (2013) Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material. FEMS Microbiol Ecol 86:101–113. doi:10.1111/1574-6941.12143
Stibal M, Šabacká M, Kaštovská K (2006) Microbial communities on glacier surfaces in Svalbard: impact of physical and chemical properties on abundance and structure of cyanobacteria and algae. Microb Ecol 52:644–654
Stomeo F et al (2012) Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated Antarctic Dry Valley. FEMS Microbiol Ecol 82:326–340. doi:10.1111/j.1574-6941.2012.01360.x
Strauss SL, Garcia-Pichel F, Day TA (2012) Soil microbial carbon and nitrogen transformations at a glacial foreland on Anvers Island, Antarctic Peninsula. Polar Biol 35:1459–1471
Strunecký O, Elster J, Komárek J (2012) Molecular clock evidence for survival of Antarctic cyanobacteria (Oscillatoriales, Phormidium autumnale) from Paleozoic times. FEMS Microbiol Ecol 82:482–490
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 32:1023–1032
Taton A, Grubisic S, Brambilla E, De Wit R, Wilmotte A (2003a) Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl Environ Microbiol 69:5157–5169
Taton A, Grubisic S, Brambilla E, De Wit R, Wilmotte A (2003b) Cyanobacterial diversity in natural and artificial microbial mats of Lake Fryxell (McMurdo Dry Valleys, Antarctica): a morphological and molecular approach. Appl Environ Microbiol 69:5157–5169
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
Thomas DN (2005) Photosynthetic microbes in freezing deserts. Trends Microbiol 13:87–88. doi:10.1016/j.tim.2004.11.002
Tolker-Nielsen T, Molin S (2000) Spatial organization of microbial biofilm communities. Microb Ecol 40:75–84
Turner J, King JC, Lachlan-Cope TA, Jones PD (2002) Climate change (communication arising): recent temperature trends in the Antarctic. Nature 418:291–292
Ugolini FC, Bockheim JG (2008) Antarctic soils and soil formation in a changing environment: a review. Geoderma 144:1–8. doi:10.1016/j.geoderma.2007.10.005
Valverde A, Makhalanyane TP, Seely M, Cowan DA (2015) Cyanobacteria drive community composition and functionality in rock-soil interface communities. Mol Ecol. doi:10.1111/mec.13068
Van Horn DJ et al (2013) Factors controlling soil microbial biomass and bacterial diversity and community composition in a cold desert ecosystem: role of geographic scale. PLoS ONE 8:e66103. doi:10.1371/journal.pone.0066103
Varin T, Lovejoy C, Jungblut AD, Vincent WF, Corbeil J (2012a) Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the High Arctic. Appl Environ Microbiol 78:549–559
Varin T, Lovejoy C, Jungblut AD, Vincent WF, Corbeil J (2012b) Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the High Arctic. Appl Environ Microbiol. doi:10.1128/AEM.06354-11
Velázquez D, Rochera C, Camacho A, Quesada A (2011) Temperature effects on carbon and nitrogen metabolism in some Maritime Antarctic freshwater phototrophic communities. Polar Biol 34:1045–1055
Verleyen E et al (2010) Structuring effects of climate-related environmental factors on Antarctic microbial mat communities. Aquat Microb Ecol 59:11–24
Vézina S, Vincent WF (1997) Arctic cyanobacteria and limnological properties of their environment: Bylot Island, Northwest Territories, Canada (73N, 80W). Polar Biol 17:523–534
Vincent WF (2000) Cyanobacterial dominance in the polar regions. The ecology of cyanobacteria. Springer, Berlin, pp 321–340
Vincent WF (2004) Microbial ecosystems of Antarctica. Cambridge University Press, Cambridge
Vincent WF (2007) Cold tolerance in cyanobacteria and life in the cryosphere. Algae and cyanobacteria in extreme environments. Springer, Berlin, pp 287–301
Vincent WF, Mueller DR, Bonilla S (2004) Ecosystems on ice: the microbial ecology of Markham Ice Shelf in the high Arctic. Cryobiology 48:103–112. doi:10.1016/j.cryobiol.2004.01.006
Vyverman W et al (2010) Evidence for widespread endemism among Antarctic micro-organisms. Polar Sci 4:103–113. doi:10.1016/j.polar.2010.03.006
Wagner C, Adrian R (2009) Cyanobacteria dominance: quantifying the effects of climate change. Limnol Oceanogr 54:2460
Wharton RA Jr, Parker BC, Simmons GM Jr (1983) Distribution, species composition and morphology of algal mats in Antarctic dry valley lakes. Phycologia 22:355–365
Wharton RA Jr, McKay CP, Simmons GM Jr, Parker BC (1985) Cryoconite holes on glaciers. Bioscience 35(8):499–503
Wood SA, Mountfort D, Selwood AI, Holland PT, Puddick J, Cary SC (2008a) Widespread distribution and identification of eight novel microcystins in antarctic cyanobacterial mats. Appl Environ Microbiol 74:7243–7251. doi:10.1128/AEM.01243-08
Wood SA, Rueckert A, Cowan DA, Cary SC (2008b) Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica. ISME J 2:308–320. doi:10.1038/ismej.2007.104
Wynn-Williams D (1996a) Antarctic microbial diversity: the basis of polar ecosystem processes. Biodivers Conserv 5:1271–1293
Wynn-Williams D (1996b) Response of pioneer soil microalgal colonists to environmental change in Antarctica. Microb Ecol 31:177–188
Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007) Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ Microbiol 9:2670–2682. doi:10.1111/j.1462-2920.2007.01379.x
Yergeau E et al (2008) Environmental microarray analyses of Antarctic soil microbial communities. Isme J 3:340–351. doi:10.1038/ismej.2008.111
Yergeau E, Hogues H, Whyte LG, Greer CW (2010) The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J 4:1206–1214
Yergeau E, Bokhorst S, Kang S, Zhou J, Greer CW, Aerts R, Kowalchuk GA (2012) Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. ISME J. doi:10.1038/ismej.2011.124
Yoshitake S, Uchida M, Koizumi H, Kanda H, Nakatsubo T (2010) Production of biological soil crusts in the early stage of primary succession on a High Arctic glacier foreland. New Phytol 186:451–460
Yung CC et al (2014) Characterization of chasmoendolithic community in Miers Valley, McMurdo Dry Valleys, Antarctica. Microb Ecol 68:351–359
Zablocki O, van Zyl L, Adriaenssens EM, Rubagotti E, Tuffin M, Cary C, Cowan D (2014) High diversity of tailed phages, eukaryotic viruses and virophage-like elements in the metaviromes of Antarctic soils. Appl Environ Microbiol 01525–01514
Zehr JP (2011) Nitrogen fixation by marine cyanobacteria. Trends Microbiol 19:162–173
Ziolkowski L, Mykytczuk N, Omelon C, Johnson H, Whyte L, Slater G (2013) Arctic gypsum endoliths: a biogeochemical characterization of a viable and active microbial community. Biogeosci Discuss 10:2269–2304
Acknowledgments
We wish to gratefully acknowledge the University of Pretoria Research Development Program (TPM), Genomics Research Institute, The National Research Foundation (NRF) of South Africa’s National Antarctic Program (SANAP program) (TPM, AV, EG. MWVG, DAC) and Ministerio de Economía y Competitividad (Spain): Grant ref CTM 2011-28736 (DV, AQ) for funding. We also wish to express our gratitude to Antarctica New Zealand for providing logistics support for our Antarctic research and Prof Craig Cary (University of Waikato NZTABS program) for facilitating access to Antarctica.
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The authors declare no conflict of interest.
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Communicated by Anurag chaurasia.
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Makhalanyane, T.P., Valverde, A., Velázquez, D. et al. Ecology and biogeochemistry of cyanobacteria in soils, permafrost, aquatic and cryptic polar habitats. Biodivers Conserv 24, 819–840 (2015). https://doi.org/10.1007/s10531-015-0902-z
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Keywords
- Cyanobacteria
- Antarctica
- Arctic
- Soil
- Aquatic
- Cryptic niches biogeochemistry