Abstract
Hardly any molecular studies have been done on euendoliths of marine coastal environments, especially along the supratidal ranges of carbonate coasts. In our study, we provide a comparative sequence analysis using 454 pyrosequencing of the 16S ribosomal RNA (rRNA) gene combined with extensive microscopy of the endolithic community from rock pools of the Croatian Adria. Molecular diversity indices and richness estimates showed high level of diversity, particularly in high-salinity samples. The most common cyanobacteria belong to the order Pleurocapsales, similar to observations on limestone coasts in other parts of the world. Using single-cell amplification sequences of Hormathonema spp., Hyella caespitosa, and Kyrtuthrix dalmatica was for the first time introduced to the public GenBank.
Microscopic investigations did not show qualitative variances in diversity among sites with different salinity but clear differences in prevalent organisms from similar environments suggesting that most of them are adapted to inhabit extreme, marine endolithic habitats and that similar species inhabit geographically separated but ecologically similar environments. This is a remarkable concordance rather seldom seen in molecular community studies in support of the hypothesis that endolithic ecosystems are seeded from a global meta-community.
The relative diversity of the community is greater than those described from harsh endolithic habitats of cold and hot deserts. The maximum likelihood phylogenetic tree consisting of 166 operational taxonomic units (OTUs) at 96 % sequence similarity revealed 11 distinct clusters. Three clusters contained only epilithic or endolithic taxa, and five clusters contained mixed epilithic and endolithic taxa. Organisms clustered according to their taxonomic affiliations and not to their preferences to salt concentrations.
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Abed RMM, de Beer D, Stief P (2015) Functional-structural analysis of nitrogen-cycle bacteria in a hypersaline mat from the Omani desert. Geom J 32:119–129
Abed RMM, Kohls K, Palinska KA, Golubic S (2010) Diversity and role of cyanobacteria and aerobic heterotrophic microorganisms in carbon cycling in arid cyanobacterial mats. In Microbial Mats, Modern and Ancient Microorganisms in Stratified Systems. In: Seckbach J, Oren A (eds) Heidelberg. Springer, New York, pp 253–273
Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253
Al-Thukair AA, Golubic S (1991) New endolithic cyanobacteria from the Arabian Gulf. I. Hyella immanis sp. Nov J Phycol 27:766–780
Al-Thukair AA, Golubic S, Rosen G (1994) New euendolithic cyanobacteria from the Bahama Bank and the Arabian Gulf: Hyella racemus sp. Nov J Phycol 30:764–769
Borin S, Crotti E, Mapelli F, Tamagnini I, Corselli C, Daffonchio D (2008) DNA is preserved and maintains transforming potential after contact with brines of the deep anoxic hyper saline lakes of the Eastern Mediterranean Sea. Saline Syst 4:1–10
De la Torre J, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of crytoendolithic communities from the Mcmurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69:3858–3867
Dell‘Anno A, Danovaro R (2005) Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science 309:2179
Ercegović A (1932) Études écologiques et sociologiques des Cyanophycées lithophytes de la còte Yougoslave de l’ Adriatique. Bull Int Acad Yougosl Sci Arts Class Sci Math Nat 26:33–56
Geitler L (1932) Cyanophyceae. In: Rabenhorst L (ed) Kryptogamen-Flora von Deutschland, Österreich und der Schweiz, 14. Akad Verlagsges, Leipzig, p 1196
Gektidis M, Golubic S (1996) A new endolithic cyanophyte/cyanobacterium: Hyella vacans sp. nov. from Lee Stocking Island, Bahamas. Nova Hedwigia 112:93–100
Gerrath J, Matthes U, Larson D (2000) Endolithic algae and cyanobacteria from cliffs of the Niagara Escarpment, Ontario, Canada. Can J Bot 78:807–815
Golubic S (1976) Organisms that build stromatolites. In: Walter MR (ed) Stromatolites. Developments in Sedimentology 20. Amsterdam: Elsevier, Chapter 4.1 pp. 113–148
Golubic S (1983) Stromatolithes, fossil and recent: a case history. In: Westbroek P, Jong EW (eds) Biomineralization and biological metal accumulation. D Reidel Publ Co, Dordrecht, pp 313–326
Golubic S, Abed RMM (2010) Entophysalis mats as environmental regulators. In: Seckbach J, Oren A (eds) Microbial mats, modern and ancient microorganisms in stratified systems. Springer, Heidelberg, New York, pp 237–251. doi:10.1007/978-90-481-3799-2_12
Golubic S, Al-Thukair AA, Gektidis M (1996) New euendolithic cyanobacteria from the Arabian Gulf and the Bahama Bank: Solentia sanguines sp. nov. Algol Stud 83:291–301
Golubic S, Brent G, Le Campion T (1970) Scanning electron microscopy of endolithic algae and fungi using a multipurpose casting-embedding technique. Lethaia 3:203–209
Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sed Petrol 51:475–478
Golubic S, Schneider J (2003) Microbial endoliths as internal biofilms. In: Krumbein WE, Dornieden T, Volkmann M (eds) Fossil and recent biofilms. Kluwer Academic Publishers, Dordrecht, pp 249–263
Gomez-Alvarez V, King GM, Nusslein K (2007) Comparative bacterial diversity in recent Hawaiian volcanic deposits of different ages. FEMS Microbiol Ecol 60:60–73
Hopley D (1982) Reef classification. Springer, Netherland
Hoppert M, Flies C, Pohl W, Günzl B, Schneider J (2004) Colonization strategies of lithobiontic microorganisms on carbonate rocks. Environ Geol 46:4212–4428
Jaag O (1945) Untersuchungen über die Vegetation und Biologie der Algen des nackten Gesteins in den Alpen, im Jura und im schweizerischen Mittelland. In Beiträge zur Kryptogamenflora der Schweiz 9: 1–560
Komárek J, Anagnostidis K (2005) Cyanoprokaryota 2. Teil/2nd Part: Oscillatoriales. In: Büdel B, Krienitz L, Gärtner G, Schagerl M (eds) Süsswasserflora von Mitteleuropa 19/2. Elsevier/Spektrum, Heidelberg, p 759
Krumbein WE, Paterson DM, Zavarzin GA (2003) Fossil and recent biofilms—a natural history of life on Earth. Kluwer Academic Publishers, Dordrecht, p 482
Lacap DC, Warren-Rhodes KA, McKay CP, Pointing SB (2011) Cyanobacteria and chloroflexi-dominated hypolithic colonization of quartz at the hyper-arid core of the Atacama Desert, Chile. Extremophiles 15:31–38
Makhalanyane TP, Valverde A, Gunnigle E, Frossard A, Ramond J-B, Cowan DA (2015) Microbial ecology of hot desert edaphic systems. FEMS Microbiol Rev 39:203–221
Marnocha CL, Dixon JC (2014) Endolithic bacterial communities in rock coatings from Kärkevagge, Swedish Lapland. FEMS Microbiol Ecol 90:533–542
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
Mills HJ, Martinez RJ, Story S, Sobecky PA (2004) Identification of members of the metabolically active microbial populations associated with Beggiatoa species mat communities from Gulf of Mexico. Appl Environ Microbiol 70:5447–5458
Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D (2007) Release and persistence of extracellular DNA in the environment. Environ Biosaf Res 6:37–53
Nogales B, Moore ER, Abraham WR, Timmis KN (1999) Identification of the metabolically active members of a bacterial community in a polychlorinated biphenyl-polluted moorland soil. Environ Microbiol 1:199–212
Norris TB, Castenholz RW (2007) Endolithic photosynthetic communities within ancient and recent travertine deposits in Yellowstone National Park. FEMS Microbiol Ecol 57:470–483
Nübel U, Garcıa-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332
Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013). vegan: Community Ecology Package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan
Palinska KA, Abed RMM, Wendt K, Charpy L, Lotocka M, Golubic S (2012) Opportunistic cyanobacteria in benthic microbial mats of a tropical lagoon, Tikehau Atoll, Tuamotu Archipelago: minor in natural populations, major in cultures. Fottea 12:127–140
Pointing SB, Chan Y, Lecap DC, Lau MCY, Jurgens JA, Farrell RL (2009) Highly specialized microbial diversity in hyper-arctic polar desert. Proc Natl Acad Sci 106:19964–19969
Radtke G, Le Campion-Alsumard T, Golubic S (1996) Microbial assemblages of the bioerosional “notch” along tropical limestone coasts. Algol Stud 83:469–482
Radtke G, Le Campion-Alsumard T, Golubic S (1997) Microbial assemblages involved in tropical coastal bioerosion: an Atlantic-Pacific comparison. Proc 8th Int Coral Reefs Symp Panama 2: 1825–1830
Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Genet Microbiol 111:1–61
Robinson CK, Wierzchos J, Black C, Crits-Christoph A, Ma B, Ravel J, Ascaso C, Artieda O, Valea S, Roldán M, Gómez-Silva B, Diruggiero J (2015) Microbial diversity and the presence of algae in halite endolithic communities are correlated to atmospheric moisture in the hyper-arid zone of the Atacama Desert. Environ Microbiol 17:299–315
Schloss PD, Handelsman J (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Schneider J (1977) Carbonate construction and decomposition by epilithic and endolithic microorganisms in salt and freshwater. In: Flugel E (ed) Fossil Algae, Recent Results and Developments. Springer, Berlin, pp 248–260
Schneider J, Le Campion-Alsumard T (1999) Construction and destruction of carbonates by marine and freshwater cyanobacteria. Eur J Phycol 34:417–426
Schneider J, Torunski H (1983) Biokarst on limestone coasts, morphogenesis and sediment production. Mar Ecol 4:45–63
Scholl DW, Taft WH (1964) Algal contribution to the formation of calcareous tufa Mono Lake California. J Sed Petrol 34:309–319
Sigler WV, Bachofen R, Zeyer J (2003) Molecular characterization of endolithic cyanobacteria inhabiting exposed dolomite in central Switzerland. Environ Microbiol 5:618–627
Silva C, Basson P, Moe R (1996) Catalogue of the Benthic Marine Algae of the Indian Ocean. Volume 79 of University of California Publications in Botany (ISBN 0-520-09810-2)
Tang Y, Lian B, Dong H, Liu D, Hou W (2012) Endolithic bacterial communities in dolomite and limestone rocks from the Nanjiang Canyon in Guizhou Karst area (China). Geomicrobiol J 29:213–225
Tribollet A, Langdon C, Golubic S, Atkinson M (2006) Endolithic microflora are major primary producers in dead carbonate substrates of Hawaiian coral reefs. J Phycol 42:292–303
Tribollet A, Radtke G, Golubic S (2011) Bioerosion. In: Reitner J, Thiel V (eds) Encyclopedia of geobiology. Encyclopedia of Earth Sciences Series, Springer, Berlin, pp 117–133
Tribollet A, Golubic S, Radtke G, Reitner J (2011b) In: Reitner N, Queric V, Arp G (eds) On Microbiocorrosion. Advances in Stromatolite Geobiology. Lecture Notes in Earth Sciences 131: 265–276
van den Hoek C, Mann DG, Jahns HM (1995) Algae: an introduction to phycology. Cambridge University Press, United Kingdom
Wade BD, Garcia-Pichel F (2003) Evaluation of DNA extraction methods for molecular analyses of microbial communities in modern microbialites. Geomicrobiol J 40:1–134
Walker JJ, Pace NR (2007) Phylogenetic composition of Rocky Mountain endolithic microbial ecosystems. Appl Environ Microbiol 73(11):3497
Whitton BA, Potts M (2000) The ecology of cyanobacteria. Kluwer Academic Publishers, Dordrecht
Wong FK, Lau MC, Lacap DC, Aitchison JC, Cowan DA, Pointing SB (2010) Endolithic microbial colonization of limestone in a high-altitude arid environment. Microb Ecol 59:689–699
Ziolkowski LA, Mykytczuk NCS, Omelon CR, Johnson H, Whyte LG, Slater GF (2013) Arctic gypsum endoliths: a biogeochemical characterization of a viable and active microbial community. Biogeosciences 10:7661–7675
Acknowledgments
Research was supported by the DFG project PA 842/9-1. International and interdisciplinary collaboration was supported and enhanced by the Hanse Institute for Advanced Studies, Delmenhorst, Germany, and by Alexander-von-Humboldt Foundation, Bad Godesberg, Germany. Special thanks are dedicated to the Dive Center Bozava.
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Brandes, M., Albach, D.C., Vogt, J.C. et al. Supratidal Extremophiles—Cyanobacterial Diversity in the Rock Pools of the Croatian Adria. Microb Ecol 70, 876–888 (2015). https://doi.org/10.1007/s00248-015-0637-0
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DOI: https://doi.org/10.1007/s00248-015-0637-0