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Bacterial and Archaeal Diversity in Hypersaline Cyanobacterial Mats Along a Transect in the Intertidal Flats of the Sultanate of Oman

  • Environmental Microbiology
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Abstract

Hypersaline intertidal zones are highly dynamic ecosystems that are exposed to multiple extreme environmental conditions including rapidly and frequently changing parameters (water, nutrients, temperature) as well as highly elevated salinity levels often caused by high temperatures and evaporation rates. Microbial mats in most extreme settings, as found at the coastline of the subtropical-arid Arabian Peninsula, have been relatively less studied compared to their counterparts around the world. We report, here, for the first time on the diversity of the bacterial and archaeal communities of marine microbial mats along an intertidal transect in a wide salt flat with strongly increased salinity employing Illumina MiSeq technology for amplicon sequencing of 16S rRNA gene fragments. Microbial communities were dominated by typical halotolerant to halophilic microorganisms, with clear shifts in community composition, richness, and diversity along the transect. Highly adapted specialists (e.g., Euhalothece, Salinibacter, Nanohaloarchaeota) were mainly found at the most extreme, upper tidal sites and less specialized organisms with wide tolerance ranges (e.g., Lyngbya, Rhodovibrio, Salisaeta, Halobacteria) in intermediate sites of the transect. The dominating taxa in the lower tidal sites were typical members of well-stabilized mats (e.g., Coleofasciculus, Anaerolineaceae, Thaumarchaeota). Up to 40% of the archaeal sequences per sample represented so far unknown phyla. In conclusion, the bacterial richness and diversity increased from upper towards lower tidal sites in line with increasing mat stabilization and functional diversity, opposed to that of cyanobacteria only and archaea, which showed their highest richness and diversity in upper tidal samples.

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References

  1. Seckbach J, Oren A (2010) Microbial mats—modern and ancient microorganisms in stratified systems. Springer Netherlands, Dordrecht. doi:10.1007/978-90-481-3799-2

    Google Scholar 

  2. Stal LJ (2012) Cyanobacterial mats and stromatolites. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer Netherlands, Dordrecht, pp. 65–125

    Chapter  Google Scholar 

  3. Golubic S (1980) Halophily and halotolerance in cyanophytes Orig Life Evol Biosph 10:169–183. doi:10.1007/BF00928667

    Article  CAS  Google Scholar 

  4. Paerl HW, Pinckney JL, Steppe TF (2000) Cyanobacterial-bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments Environ Microbiol 2:11–26. doi:10.1046/j.1462-2920.2000.00071.x

    Article  CAS  PubMed  Google Scholar 

  5. Benlloch S, López-López A, Casamayor EO, Øvreås L, Goddard V, Daae FL, Smerdon G, Massana R, Joint I, Thingstad F, Pedrós-Alió C, Rodríguez-Valera F (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern Environ Microbiol 4:349–360. doi:10.1046/j.1462-2920.2002.00306.x

    Article  PubMed  Google Scholar 

  6. Bolhuis H, Cretoiu MS, Stal LJ (2014) Molecular ecology of microbial mats FEMS Microbiol Ecol 90:335–350. doi:10.1111/1574-6941.12408

    CAS  PubMed  Google Scholar 

  7. Ventosa A, de la Haba RR, Sánchez-Porro C, Papke RT (2015) Microbial diversity of hypersaline environments: a metagenomic approach Curr Opin Microbiol 25:80–87. doi:10.1016/j.mib.2015.05.002

    Article  CAS  PubMed  Google Scholar 

  8. Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification Hydrol Earth Syst Sci 11:1633–1644. doi:10.5194/hess-11-1633-2007

    Article  Google Scholar 

  9. Abed RMM, Kohls K, Schoon R, Scherf AK, Schacht M, Palinska KA, Al-Hassani H, Hamza W, Rullkötter J, Golubic S (2008) Lipid biomarkers, pigments and cyanobacterial diversity of microbial mats across intertidal flats of the arid coast of the Arabian Gulf (Abu Dhabi, UAE) FEMS Microbiol Ecol 65:449–462. doi:10.1111/j.1574-6941.2008.00537.x

    Article  CAS  PubMed  Google Scholar 

  10. Oren A (2015) Cyanobacteria in hypersaline environments: biodiversity and physiological properties Biodivers Conserv 24:781–798. doi:10.1007/s10531-015-0882-z

    Article  Google Scholar 

  11. Allen MA, Goh F, Burns BP, Neilan BA (2009) Bacterial, archaeal and eukaryotic diversity of smooth and pustular microbial mat communities in the hypersaline lagoon of Shark Bay Geobiology 7:82–96. doi:10.1111/j.1472-4669.2008.00187.x

    Article  CAS  PubMed  Google Scholar 

  12. Schneider D, Arp G, Reimer A, Reitner J, Daniel R (2013) Phylogenetic analysis of a microbialite-forming microbial mat from a hypersaline lake of the Kiritimati Atoll, Central Pacific PLoS One 8:e66662. doi:10.1371/journal.pone.0066662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Robertson CE, Spear JR, Harris JK, Pace NR (2009) Diversity and stratification of archaea in a hypersaline microbial mat Appl Environ Microbiol 75:1801–1810. doi:10.1128/AEM.01811-08

    Article  CAS  PubMed  Google Scholar 

  14. Abed RMM, Kohls K, de Beer D (2007) Effect of salinity changes on the bacterial diversity, photosynthesis and oxygen consumption of cyanobacterial mats from an intertidal flat of the Arabian Gulf Environ Microbiol 9:1384–1392. doi:10.1111/j.1462-2920.2007.01254.x

    Article  CAS  PubMed  Google Scholar 

  15. Abed RMM, Klempová T, Gajdos P, Certík M (2015) Bacterial diversity and fatty acid composition of hypersaline cyanobacterial mats from an inland desert wadi J Arid Environ 115:81–89. doi:10.1016/j.jaridenv.2015.01.010

    Article  Google Scholar 

  16. Harris JK, Caporaso JG, Walker JJ, Spear JR, Gold NJ, Robertson CE, Hugenholtz P, Goodrich J, McDonald D, Knights D, Marshall P, Tufo H, Knight R, Pace NR (2013) Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat ISME J 7:50–60. doi:10.1038/ismej.2012.79

    Article  PubMed  Google Scholar 

  17. Javor B (1989) Hypersaline environments—microbiology and biogeochemistry. doi: 10.1007/978-3-642-74370-2

  18. Oren A (2012) Salts and brines. In: Whitton AB (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer Netherlands, Dordrecht, pp. 401–426

    Chapter  Google Scholar 

  19. Vavourakis CD, Ghai R, Rodriguez-Valera F, Sorokin DY, Tringe SG, Hugenholtz P, Muyzer G (2016) Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines Front Microbiol. doi:10.3389/fmicb.2016.00211

  20. Bolhuis H, Stal LJ (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing ISME J 5:1701–1712. doi:10.1038/ismej.2011.52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Al-Thukair AA, Al-Hinai K (1993) Preliminary damage assessment of algal mats sites located in the Western Gulf following the 1991 oil spill Mar Pollut Bull 27:229–238

    Article  Google Scholar 

  22. Al-Zaidan ASY, Kennedy H, Jones DA, Al-Mohanna SY (2006) Role of microbial mats in Sulaibikhat Bay (Kuwait) mudflat food webs: evidence from δ13C analysis Mar Ecol Prog Ser 308:27–36. doi:10.3354/meps308027

    Article  CAS  Google Scholar 

  23. Abed RMM, Al-Thukair A, De Beer D (2006) Bacterial diversity of a cyanobacterial mat degrading petroleum compounds at elevated salinities and temperatures FEMS Microbiol Ecol 57:290–301. doi:10.1111/j.1574-6941.2006.00113.x

    Article  CAS  PubMed  Google Scholar 

  24. Abed RMM, Zein B, Al-Thukair A, de Beer D (2007) Phylogenetic diversity and activity of aerobic heterotrophic bacteria from a hypersaline oil-polluted microbial mat Syst Appl Microbiol 30:319–330. doi:10.1016/j.syapm.2006.09.001

    Article  CAS  PubMed  Google Scholar 

  25. Al Hasan RH, Sorkhoh NA, Al Bader D, Radwan SS (1994) Utilization of hydrocarbons by cyanobacteria from microbial mats on oily coasts of the gulf Appl Microbiol Biotechnol 41:615–619. doi:10.1007/BF00178499

    Article  Google Scholar 

  26. Sørensen KB, Canfield DE, Teske AP, Oren A (2005) Community composition of a hypersaline endoevaporitic microbial mat Appl Environ Microbiol 71:7352–7365. doi:10.1128/AEM.71.11.7352

    Article  PubMed  PubMed Central  Google Scholar 

  27. Sarazin G, Michard G, Prevot F (1999) A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples Water Res 33:290–294

    Article  CAS  Google Scholar 

  28. Benesch R, Mangelsdorf P (1972) Eine Methode zur colorimetrischen Bestimmung von Ammoniak in Meerwasser Helgoländer Meeresun 23:365–375. doi:10.1007/BF01609682

    Article  CAS  Google Scholar 

  29. Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite Nitric Oxide Biol Chem 5:62–71. doi:10.1006/niox.2000.0319

    Article  CAS  Google Scholar 

  30. Schnetger B, Lehners C (2014) Determination of nitrate plus nitrite in small volume marine water samples using vanadium(III)chloride as a reduction agent Mar Chem 160:91–98. doi:10.1016/j.marchem.2014.01.010

    Article  CAS  Google Scholar 

  31. O’Dell JW (1993) Method 365.1, Revision 2.0: determination of phosphorus by semi-automated colorimetry. EPA - United States Environ Prot Agency, 1–15

  32. Itaya K, Ul M (1966) A new micromethod for the colorimetric determination of inorganic phosphate Clin Chim Acte 14:361–366. doi:10.1016/0009-8981(66)90114-8

    Article  CAS  Google Scholar 

  33. Altmann HJ, Fürstenau E, Gielewski A, Scholz L (1971) Photometrische Bestimmung kleiner Phosphatmengen mit Malachitgrün Fresenius’ Zeitschrift für Anal Chemie 256:274–276. doi:10.1007/BF00537892

    Article  CAS  Google Scholar 

  34. Komárek J (2013) Süßwasserflora von Mitteleuropa, Bd. 19/3: Cyanoprokaryota. 3. Teil / 3rd part: Heterocytous Genera. Springer Spektrum

  35. Komárek J (2008) Süßwasserflora von Mitteleuropa, Bd. 19/1: Cyanoprokaryota. 1. Teil / 1st part: Chroococcales. Springer Spektrum

  36. Komárek J, Anagnostidis K (2007) Süßwasserflora von Mitteleuropa, Bd. 19/2: Cyanoprokaryota. 2. Teil / 2nd part: Oscillatoriales. Springer Spektrum

  37. Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria Appl Environ Microbiol 63:3327–3332

    PubMed  PubMed Central  Google Scholar 

  38. Wilmotte A, Demonceau C, Goffart A, Hecq J-H, Demoulin V, Crossley AC (2002) Molecular and pigment studies of the picophytoplankton in a region of the Southern Ocean (42–54° S, 141–144° E) in March 1998 Deep Sea Res II Top Stud Oceanogr 49:3351–3363. doi:10.1016/S0967-0645(02)00087-5

    Article  CAS  Google Scholar 

  39. Herlemann DPR, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea ISME J 5:1571–1579. doi:10.1038/ismej.2011.41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers J Microbiol Methods 55:541–555. doi:10.1016/j.mimet.2003.08.009

    Article  CAS  PubMed  Google Scholar 

  41. Burggraf S, Huber H, Stetter KO (1997) Reclassification of the Crenarchaeal orders and families in accordance with 16S rRNA sequence data Int J Syst Bacteriol 47:657–660. doi:10.1099/00207713-47-3-657

    Article  CAS  PubMed  Google Scholar 

  42. 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. doi:10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Nucleic Acids Res 41:D590–D596. doi:10.1093/nar/gks1219

    Article  CAS  PubMed  Google Scholar 

  44. 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. doi:10.1128/AEM.00062-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences J Comput Biol 7:203–214. doi:10.1089/10665270050081478

    Article  CAS  PubMed  Google Scholar 

  46. Garrity GM, Boone DR, Castenholz RW (2001) Bergey’s Manual of Systematic Bacteriology. Volume one, The Archaea and the Deeply Branching and Phototrophic Bacteria, 2. doi:10.1007/978-0-387-21609-6

  47. Garrity GM, Brenner DJ, Krieg NR, Staley JT (2005) Bergey’s Manual of Systematic Bacteriology. Volume Two, The Proteobacteria, Part B, The Gammaproteobacteria, 2. doi: 10.1007/0-387-28022-7

  48. Garrity GM, Brenner DJ, Krieg NR, Staley JT (2005) Bergey’s Manual of Systematic Bacteriology. Volume Two, The Proteobacteria, Part C, The Alpha-, Beta-, Delta-, and Epsilonproteobacteria, 2. doi: 10.1007/0-387-29298-5

  49. Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K-H, Whitman WB (2009) Bergey’s Manual of Systematic Bacteriology. Volume Three, The Firmicutes, 2. doi: 10.1007/978-0-387-68489-5

  50. Krieg NR, Ludwig W, Whitman W, Hedlund BP, Paster BJ, Staley JT, Ward N, Brown D, Parte A (2010) Bergey’s Manual of Systematic Bacteriology. Volume Four, The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes, 2. doi: 10.1007/978-0-387-68572-4

  51. Whitman WB, Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Ludwig W, Suzuki K-I, Parte AC (2012) Bergey’s Manual of Systematic Bacteriology, Volumen Five, The Actinobacteria, 2. doi: 10.1007/978-0-387-68233-4

  52. Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology Annu Rev Ecol Evol Syst 36:519–539. doi:10.1146/annurev.ecolsys.36.102803.095431

    Article  Google Scholar 

  53. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  54. Oren A (2006) Life at high salt concentrations. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The Prokaryotes: Volume 2: Ecophysiology and Biochemistry. Springer New York, New York, pp. 263–282

    Google Scholar 

  55. Oren A, Sørensen KB, Canfield DE, Teske AP, Ionescu D, Lipski A, Altendorf K (2009) Microbial communities and processes within a hypersaline gypsum crust in a saltern evaporation pond (Eilat, Israel) Hydrobiologia 626:15–26. doi:10.1007/s10750-009-9734-8

    Article  CAS  Google Scholar 

  56. Vogt JC, Albach DC, Palinska KA (2017) Cyanobacteria of the Wadden Sea—seasonality and sediment influence on community composition. Hydrobiologia. doi:10.1007/s10750-017-3287-z

  57. Billerbeck M, Røy H, Bosselmann K, Huettel M (2007) Benthic photosynthesis in submerged Wadden Sea intertidal flats Estuar Coast Shelf Sci 71:704–716. doi:10.1016/j.ecss.2006.09.019

    Article  Google Scholar 

  58. Karsten U, Maier J, Garcia-Pichel F (1998) Seasonality in UV-absorbing compounds of cyanobacterial mat communities from an intertidal mangrove flat Aquat Microb Ecol 16:37–44. doi:10.3354/ame016037

    Article  Google Scholar 

  59. Castenholz RW, Garcia-Pichel F (2012) Cyanobacterial responses to UV radiation. In: Whitton AB (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer Netherlands, Dordrecht, pp. 481–499

    Chapter  Google Scholar 

  60. Rothrock Jr MJ, Garcia-Pichel F (2005) Microbial diversity of benthic mats along a tidal desiccation gradient Environ. Microbiol. 7:593–601. doi:10.1111/j.1462-2920.2004.00728.x

    Article  CAS  PubMed  Google Scholar 

  61. Normand P, Caumette P, Goulas P, Pujic P, Wisniewski-Dyé F (2015) Adaptations of prokaryotes to their biotopes and to physicochemical conditions in natural or anthropized environments. In: Bertrand J-C, Caumette P, Lebaron P, Matheron R, Normand P, Sime-Ngando T (eds) Environmental microbiology: fundamentals and applications: microbial ecology. Springer Netherlands, Dordrecht, pp. 293–351

    Google Scholar 

  62. Krumbein WE, Paterson DM, Stal LJ (1994) Biostabilization of sediments. Bibliotheks- und Informationssystem der Universität Oldenburg (bis)-Verlag, Oldenburg

    Google Scholar 

  63. Garcia-Pichel F, Nübel U, Muyzer G (1998) The phylogeny of unicellular, extremely halotolerant cyanobacteria Arch Microbiol 169:469–482. doi:10.1007/s002030050599

    Article  CAS  PubMed  Google Scholar 

  64. Potts M (1994) Desiccation tolerance of prokaryotes Microbiol Rev 58:755–805. doi:10.1093/icb/45.5.800

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Garcia-Pichel F, Prufert-Bebout L, Muyzer G (1996) Phenotypic and phylogenetic analyses show Microcoleus chthonoplastes to be a cosmopolitan cyanobacterium Appl. Environ. Microbiol. 62:3284–3291

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Siegesmund MA, Johansen JR, Karsten U, Friedl T (2008) Coleofasciculus gen. nov. (Cyanobacteria): morphological and molecular criteria for revision of the genus Microcoleus Gomont J Phycol 44:1572–1585. doi:10.1111/j.1529-8817.2008.00604.x

    Article  PubMed  Google Scholar 

  67. Abed RMM, Garcia-Pichel F, Hernández-Mariné M (2002) Polyphasic characterization of benthic, moderately halophilic, moderately thermophilic cyanobacteria with very thin trichomes and the proposal of Halomicronema excentricum gen. nov., sp. nov Arch. Microbiol. 177:361–370. doi:10.1007/s00203-001-0390-2

    Article  CAS  PubMed  Google Scholar 

  68. Kirkwood AE, Buchheim JA, Buchheim MA, Henley WJ (2008) Cyanobacterial diversity and halotolerance in a variable hypersaline environment Microb Ecol 55:453–465. doi:10.1007/s00248-007-9291-5

    Article  PubMed  Google Scholar 

  69. Castenholz RW, Wilmotte A, Herdman M, Rippka R, Waterbury JB, Iteman I, Hoffmann L (2001) Phylum BX. Cyanobacteria. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology: volume one: the archaea and the deeply branching and phototrophic bacteria. Springer New York, New York, pp. 473–599

    Google Scholar 

  70. Nübel U, Garcia-Pichel F, Clavero E, Muyzer G (2000) Matching molecular diversity and ecophysiology of benthic cyanobacteria and diatoms in communities along a salinity gradient Environ. Microbiol. 2:217–226. doi:10.1046/j.1462-2920.2000.00094.x

    Article  PubMed  Google Scholar 

  71. de Wit R, van Boekel WHM, van Germerden H (1988) Growth of the cyanobacterium Microcoleus chtonoplastes on sulfide FEMS Microbiol Ecol 53:203–210. doi:10.1111/j.1574-6968.1988.tb02665.x

    Article  Google Scholar 

  72. Jørgensen BB, Cohen Y, Revsbech NP (1986) Transition from anoxygenic to oxygenic photosynthesis in a Microcoleus chthonoplastes cyanobacterial mat Appl Environ Microbiol 51:408–417

    PubMed  PubMed Central  Google Scholar 

  73. Moezelaar R, Bijvank SM, Stal LJ (1996) Fermentation and sulfur reduction in the mat-building cyanobacterium Microcoleus chthonoplastes Appl Environ Microbiol 62:1752–1758

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Kohls K, Abed RMM, Polerecky L, Weber M, de Beer D (2010) Halotaxis of cyanobacteria in an intertidal hypersaline microbial mat Environ Microbiol 12:567–575. doi:10.1111/j.1462-2920.2009.02095.x

    Article  CAS  PubMed  Google Scholar 

  75. Pearson HW, Howsley R, Kjeldsen CK, Walsby AE (1979) Aerobic nitrogenase activity associated with a non-heterocystous filamentous cyanobacterium FEMS Microbiol Lett 5:163–167. doi:10.1111/j.1574-6968.1979.tb03271.x

    Article  CAS  Google Scholar 

  76. Bolhuis H, Severin I, Confurius-Guns V, Wollenzien UIA, Stal LJ (2010) Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium Microcoleus chthonoplastes ISME J 4:121–130. doi:10.1038/ismej.2009.99

    Article  CAS  PubMed  Google Scholar 

  77. Sroga GE (1997) Regulation of nitrogen fixation by different nitrogen sources in the filamentous non-heterocystous cyanobacterium Microcoleus sp FEMS Microbiol Lett 153:11–15. doi:10.1111/j.1574-6968.1997.tb10457.x

    Article  CAS  PubMed  Google Scholar 

  78. Lundgren P, Bauer K, Lugomela C, Söderbäck E, Bergman B (2003) Reevaluation of the nitrogen fixation behavior in the marine non-heterocystous cyanobacterium Lyngbya majuscula J. Phycol. 39:310–314

    Article  CAS  Google Scholar 

  79. Stal LJ, Severin I, Bolhuis H (2010) The ecology of nitrogen fixation in cyanobacterial mats. In: Hallenbeck CP (ed) Recent advances in phototrophic prokaryotes. Springer New York, New York, pp. 31–45

    Chapter  Google Scholar 

  80. Woebken D, Burow LC, Behnam F, Mayali X, Schintlmeister A, Fleming ED, Prufert-Bebout L, Singer SW, López Cortés A, Hoehler TM, Pett-Ridge J, Spormann AM, Wagner M, Weber PK, Bebout BM (2015) Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach ISME J 9:485–496. doi:10.1038/ismej.2014.144

    Article  CAS  PubMed  Google Scholar 

  81. Walsby AE, Van Rijn J, Cohen Y (1983) The biology of a new gas-vacuolate cyanobacterium, Dactylococcopsis salina sp. nov., in Solar Lake Proc R Soc Lond Ser B Biol Sci 217:417 LP–417447

    Article  Google Scholar 

  82. Antón J, Oren A, Benlloch S, Rodríguez-Valera F, Amann R, Rosselló-Mora R (2002) Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the bacteria from saltern crystallizer ponds Int J Syst Evol Microbiol 52:485–491. doi:10.1099/ijs.0.01913-0

    Article  PubMed  Google Scholar 

  83. Makhdoumi-Kakhki A, Amoozegar MA, Ventosa A (2012) Salinibacter iranicus sp. nov. and Salinibacter luteus sp. nov., isolated from a salt lake, and emended descriptions of the genus Salinibacter and of Salinibacter ruber Int J Syst Evol Microbiol 62:1521–1527. doi:10.1099/ijs.0.031971-0

    Article  CAS  PubMed  Google Scholar 

  84. Oren A, Heldal M, Norland S, Galinski EA (2002) Intracellular ion and organic solute concentrations of the extremely halophilic bacterium Salinibacter ruber Extremophiles 6:491–498. doi:10.1007/s00792-002-0286-3

    Article  CAS  PubMed  Google Scholar 

  85. Oren A (2013) Salinibacter: an extremely halophilic bacterium with archaeal properties FEMS Microbiol. Lett. 342:1–9. doi:10.1111/1574-6968.12094

    Article  CAS  PubMed  Google Scholar 

  86. Vaisman N, Oren A (2009) Salisaeta longa gen. nov., sp. nov., a red, halophilic member of the Bacteroidetes Int J Syst Evol Microbiol 59:2571–2574. doi:10.1099/ijs.0.010892-0

    Article  CAS  PubMed  Google Scholar 

  87. Imhoff JF, Petri R, Süling J (1998) Reclassification of species of the spiral-shaped phototrophic purple non-sulfur bacteria of the α-Proteobacteria: description of the new genera Phaeospirillum gen. nov., Rhodovibrio gen. nov., Rhodothalassium gen. nov. and Roseospira gen. nov. as well as transfer of Rhodospirillum fulvum to Phaeospirillum fulvum comb. nov., of Rhodospirillum molischianum to Phaeospirillum molischianum comb. nov., of Rhodospirillum salinarum to Rhodovibrio salinarum comb. nov., of Rhodospirillum sodomense to Rhodovibrio sodomensis comb. nov., of Rhodospirillum salexigens to Rhodothalassium salexigens comb. nov. and of Rhodospirillum mediosalinum to Roseospira mediosalina comb. nov Int J Syst Bacteriol 48:793–798. doi:10.1099/00207713-48-3-793

    Article  PubMed  Google Scholar 

  88. Baldani JI, Videira SS, dos Santos Teixeira KR, Reis VM, Martinez de Oliveira AL, Schwab S, Maltempi de Souza E, Pedraza RO, Baldani VLD, Hartmann A (2014) The family Rhodospirillaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: alphaproteobacteria and Betaproteobacteria. Springer Berlin Heidelberg, Berlin, pp. 533–618

    Chapter  Google Scholar 

  89. Liu H, Buskey EJ (2000) Hypersalinity enhances the production of extracellular polymeric substance (EPS) in the texas brown tide alga, Aureoumbra lagunensis (Pelagophyceae) J. Phycol. 36:71–77. doi:10.1046/j.1529-8817.2000.99076.x

    Article  CAS  Google Scholar 

  90. Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly FEMS Microbiol Rev 33:917–941. doi:10.1111/j.1574-6976.2009.00183.x

    Article  CAS  PubMed  Google Scholar 

  91. Chen L-Z, Li D-H, Song L-R, Hu C-X, Wang G-H, Liu Y-D (2006) Effects of salt stress on carbohydrate metabolism in desert soil alga Microcoleus vaginatus Gom J Integr Plant Biol 48:914–919. doi:10.1111/j.1744-7909.2006.00291.x

    Article  CAS  Google Scholar 

  92. McKew BA, Dumbrell AJ, Taylor JD, McGenity TJ, Underwood GJC (2013) Differences between aerobic and anaerobic degradation of microphytobenthic biofilm-derived organic matter within intertidal sediments FEMS Microbiol Ecol 84:495–509. doi:10.1111/1574-6941.12077

    Article  CAS  PubMed  Google Scholar 

  93. Helm RF, Potts M (2012) Extracellular Matrix (ECM). In: Whitton AB (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer Netherlands, Dordrecht, pp. 461–480

    Chapter  Google Scholar 

  94. Jonkers HM, Abed RMM (2003) Identification of aerobic heterotrophic bacteria from the photic zone of a hypersaline microbial mat Aquat Microb Ecol 30:127–133. doi:10.3354/ame030127

    Article  Google Scholar 

  95. Mack EE, Mandelco L, Woese CR, Madigan MT (1993) Rhodospirillum sodomense, sp. nov., a Dead Sea Rhodospirillum species Arch Microbiol 160:363–371

    Article  CAS  Google Scholar 

  96. Tkavc R, Gostinčar C, Turk M, Visscher PT, Oren A, Gunde-Cimerman N (2011) Bacterial communities in the “petola” microbial mat from the Sečovlje salterns (Slovenia) FEMS Microbiol. Ecol. 75:48–62. doi:10.1111/j.1574-6941.2010.00985.x

    Article  CAS  PubMed  Google Scholar 

  97. Krekeler D, Sigalevich P, Teske A, Cypionka H, Cohen Y (1997) A sulfate reducing bacterium from the oxic layer of a microbial mat from Solar Lake (Sinai), Desulfovibrio oxyclinae sp. nov Arch Microbiol 167:369–375. doi:10.1007/s002030050457

    Article  CAS  Google Scholar 

  98. Ward NL (2010) Phylum XXV. Planctomycetes Garrity and Holt 2001, 137 emend. Ward (this volume). In: Krieg NR, Ludwig W, Whitman W, Hedlund BP, Paster BJ, Staley JT, Ward N, Brown D, Parte A (eds) Bergey’s manual of systematic bacteriology, volume four, the Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. Springer New York, New York, pp. 879–925

    Google Scholar 

  99. Schlesner H, Rensmann C, Tindall BJ, Gade D, Rabus R, Pfeiffer S, Hirsch P (2004) Taxonomic heterogeneity within the Planctomycetales as derived by DNA-DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Perillula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov. an Int J Syst Evol Microbiol 54:1567–1580. doi:10.1099/ijs.0.63113-0

    Article  CAS  PubMed  Google Scholar 

  100. Roh S-W, Lee H-W, Yim KJ, Shin N-R, Lee J, Whon TW, Lim N-L, Kim D, Bae J-W (2013) Rhodopirellula rosea sp. nov., a novel bacterium isolated from an ark clam Scapharca broughtonii J Microbiol 51:301–304. doi:10.1007/s12275-013-3210-x

    Article  CAS  PubMed  Google Scholar 

  101. Bondoso J, Albuquerque L, Lobo-da-Cunha A, da Costa MS, Harder J, Lage OM (2014) Rhodopirellula lusitana sp. nov. and Rhodopirellula rubra sp. nov., isolated from the surface of macroalgae Syst Appl Microbiol 37:157–164. doi:10.1016/j.syapm.2013.11.004

    Article  CAS  PubMed  Google Scholar 

  102. Lee H-W, Roh SW, Shin N-R, Lee J, Whon TW, Jung M-J, Yun J-H, Kim M-S, Hyun D-W, Kim D, Bae J-W (2013) Blastopirellula cremea sp. nov., isolated from a dead ark clam Int J Syst Evol Microbiol 63:2314–2319. doi:10.1099/ijs.0.044099-0

    Article  CAS  PubMed  Google Scholar 

  103. Yoon J, Jang J-H, Kasai H (2014) Algisphaera agarilytica gen. nov., sp. nov., a novel representative of the class Phycisphaerae within the phylum Planctomycetes isolated from a marine alga. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 105:317–324. doi:10.1007/s10482-013-0076-1

    CAS  Google Scholar 

  104. Yoon J, Matsuo Y, Kasai H, Lee M-K (2015) Phylogenetic and taxonomic analyses of Rhodopirellula caenicola sp. nov., a new marine Planctomycetes species isolated from iron sand J Phylogenetics Evol Biol. doi:10.4172/2329-9002.1000143

  105. Oren A (2014) The family Halobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: other major lineages of bacteria and the archaea. Springer Berlin Heidelberg, Berlin, pp. 41–121

    Google Scholar 

  106. Cui H-L, Zhang W-J (2014) Salinigranum rubrum gen. nov., sp. nov., a member of the family Halobacteriaceae isolated from a marine solar saltern Int J Syst Evol Microbiol 64:2029–2033. doi:10.1099/ijs.0.061606-0

    Article  CAS  PubMed  Google Scholar 

  107. Song HS, Cha I-T, Yim KJ, Lee H-W, Hyun D-W, Lee S-J, Rhee S-K, Kim K-N, Kim D, Choi J-S, Seo M-J, Choi H-J, Bae J-W, Rhee J-K, Nam Y-D, Roh SW (2014) Halapricum salinum gen. nov., sp. nov., an extremely halophilic archaeon isolated from non-purified solar salt. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 105:925–932. doi:10.1007/s10482-014-0147-y

    Google Scholar 

  108. Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology Curr Opin Microbiol 14:300–306. doi:10.1016/j.mib.2011.04.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Zehr JP, Kudela RM (2011) Nitrogen cycle of the open ocean: from genes to ecosystems Annu Rev Mar Sci 3:197–225. doi:10.1146/annurev-marine-120709-142819

    Article  Google Scholar 

  110. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils Nature 442:806–809. doi:10.1038/nature04983

    Article  CAS  PubMed  Google Scholar 

  111. Reysenbach A-L, Brileya K (2014) The family Thermoplasmataceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: other major lineages of bacteria and the archaea. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 385–387

    Google Scholar 

  112. Grime JP (1973) Competitive exclusion in herbaceous vegetation Nature 242:344–347. doi:10.1038/242344a0

    Article  Google Scholar 

  113. Colwell RK, Hurtt GC (1994) Nonbiological gradients in species richness and a spurious rapoport effect Am Nat 144:570–595. doi:10.2307/2462939

    Article  Google Scholar 

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Acknowledgements

We thank the Hanse-Wissenschaftskolleg (HWK), Institute for Advanced Study, in Delmenhorst, Germany, and the study group (RA) for supporting cooperation as well as Carola Lehners (Microbiogeochemistry group, Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University Oldenburg) and Daniela Meißner (Landscape Ecology group, Institute of Biology and Environmental Sciences, University of Oldenburg) for their technical support and the possibility to conduct the measurements of abiotic parameters in their laboratory. This work was supported by the German Research Foundation (DFG) [project PA 842/9-1].

Sequence Data

Representative sequences of all OTUs were deposited in GenBank (https://www.ncbi.nlm.nih.gov/Genbank/) with accession numbers KY343476-KY343956 (cyanobacteria), KY342699-KY343475 (bacteria), and KY343957-KY344275 (archaea).

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Author notes

  1. Katarzyna A. Palinska

    Present address: Institute of Oceanography, Faculty of Oceanography and Geography, University of Gdansk, Al. J. Pilsudskiego 46, 80-378, Gdynia, Poland

Authors and Affiliations

  1. Institute for Biology and Environmental Science (IBU), Plants Biodiversity and Evolution, Carl-von-Ossietzky University of Oldenburg, Carl-von-Ossietzky-Str. 9-11, 26129, Oldenburg, Germany

    Janina C. Vogt, Dirk C. Albach & Katarzyna A. Palinska

  2. Biology Department, College of Science, Sultan Qaboos University, P.O. Box 36, 123, Al Khoud, Oman

    Raeid M. M. Abed

Authors
  1. Janina C. Vogt
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  2. Raeid M. M. Abed
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  3. Dirk C. Albach
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  4. Katarzyna A. Palinska
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Corresponding author

Correspondence to Janina C. Vogt.

Electronic supplementary material

Online Resource 1

Linear regression analyses of abiotic factors: (a-c) Percent of grain size fractions and (d) the thickness of salt crust (O1-O5) as well as (e) salinity, (f) pH, (g) total alkalinity (TA) and (h-l) nutrient concentrations of porewater samples (O2-O5); sampling of porewater was not possible at sampling site O1; the overlaying water (OW) had 18% salinity and concentrations of 3.6 mM TA, 34.1 μM NH4, 2.0 μM PO4, 2.6 μM NOx, 0.3 μM NO2, 2.6 μM NO3 (GIF 35 kb)

High resolution image (TIFF 28477 kb)

Online Resource 2

Rarefaction curves for the entire datasets (a) and per dataset for each sample (b-d) (GIF 19 kb)

High resolution image (TIFF 13289 kb)

Online Resource 3

Total OTU and sequence numbers (numOtus, num seqs) per sample and assay and taxonomic classification as well as relative sequence abundance of all OTUs per assay that where shared by all samples based on the total sequence numbers per sample (PDF 469 kb)

Online Resource 4a

Sequence numbers per assay, sample and OTU as well as taxonomic classification per OTU according to the reference dataset (Silva/herdman cyanophylo) for the cyanobacterial dataset. (PDF 396 kb)

Online Resource 4b

Sequence numbers per assay, sample and OTU as well as taxonomic classification per OTU according to the reference dataset (Silva/herdman cyanophylo) and functional classification for the bacterial dataset. (PDF 456 kb)

Online Resource 4c

Sequence numbers per assay, sample and OTU as well as taxonomic classification per OTU according to the reference dataset (Silva/herdman cyanophylo) for the archaeal dataset (PDF 427 kb)

Online Resource 5

OTU numbers of prevailing taxonomic groups of the cyanobacterial, bacterial and archaeal dataset (PDF 359 kb)

Online Resource 6

Relative sequence abundances of cyanobacterial sequences detected within the specific cyanobacterial (a, c) and the universal bacterial (b, d) sequencing assay; cyanobacterial sequences were classified to order (a, b) and genus (c, d) level; both datasets were clustered at 97% similarity level and OTUs ≤10 sequences were removed (TIFF 15969 kb)

High resolution image (TIFF 15969 kb)

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Vogt, J.C., Abed, R.M.M., Albach, D.C. et al. Bacterial and Archaeal Diversity in Hypersaline Cyanobacterial Mats Along a Transect in the Intertidal Flats of the Sultanate of Oman. Microb Ecol 75, 331–347 (2018). https://doi.org/10.1007/s00248-017-1040-9

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