Advertisement

Phototrophic Microbial Mats

  • Lucas J. Stal
  • Henk Bolhuis
  • Mariana Silvia Cretoiu
Chapter

Abstract

Microbial mats are structured, small-scale microbial ecosystems, and similar as biofilms cover a substratum like a tissue. A general characteristic of a microbial mat is the steep physicochemical gradients that are the result of the metabolic activities of the mat microorganisms. Virtually every microbial mat is formed through autotrophic metabolism and through the fixation of atmospheric dinitrogen. Chemoautotrophic organisms fuel these processes in the absence of light. In illuminated environments photoautotrophic organisms are the driving force and these mats are subject of this chapter. In the vast majority of cases, primary production by the oxygenic phototrophic cyanobacteria is the basis of a diverse community that forms a living entity with a macroscopic habitus. This entity has its own physiology that is the result of interaction, communication, cooperation, and competition of the individual functional groups of microorganisms. Organic matter is remineralized and in sulfur-dominated environments sulfate-reducing bacteria are responsible for end-oxidation that leads to the production of sulfide, which is used by anoxygenic photoautotrophic bacteria. Aerobic and anaerobic anoxygenic phototrophic bacteria and proteorhodopsin-containing bacteria are important as secondary producers and take care of the decomposition of organic matter in a process that is aided by light.

Keywords

Green Sulfur Bacterium Purple Sulfur Bacterium Ebro Delta Anoxygenic Phototrophic Bacterium Anoxygenic Photosynthesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The research has received funding from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement n° 311975. This publication reflects the views only of the authors, and the European Union cannot be held responsible for any use, which may be made of the information contained therein.

References

  1. Bak F, Pfennig N (1987) Chemolithotrophic growth of Desulfovibrio sulfodismutans sp. nov. by disproportionation of inorganic sulfur compounds. Arch Microbiol 147:184–189CrossRefGoogle Scholar
  2. Bebout BM, Garcia-Pichel F (1995) UV B-induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol 61:4215–4222PubMedPubMedCentralGoogle Scholar
  3. 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 5:1701–1712PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bolhuis H, Cretoiu MS, Stal LJ (2014) Molecular ecology of microbial mats. FEMS Microbiol Ecol 90:335–350PubMedGoogle Scholar
  5. 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. The ISME J 4:121–130Google Scholar
  6. Brauer VS, Stomp M, Bouvier T, Fouilland E, Leboulanger C, Confurius-Guns V, Weissing FJ, Stal LJ, Huisman J (2015) Competition and facilitation between the marine nitrogen-fixing cyanobacterium Cyanothece and its associated bacterial community. Front Microbiol 5:795PubMedPubMedCentralCrossRefGoogle Scholar
  7. Burow LC, Woebken D, Bebout BM, McMurdie PJ, Singer SW, Pett-Ridge J, Prufert-Bebout L, Spormann AM, Weber PK, Hoehler TM (2012) Hydrogen production in photosynthetic microbial mats in the Elkhorn Slough estuary, Monterey Bay. ISME J 6:863–874PubMedCrossRefGoogle Scholar
  8. Campbell SE (1979) Soil stabilization by a prokaryotic desert crust: implications for Precambrian land biota. Orig Life 9:335–348PubMedCrossRefGoogle Scholar
  9. Canfield DE, Des Marais DJ (1991) Aerobic sulfate reduction in microbial mats. Science 251:1471–1473PubMedCrossRefGoogle Scholar
  10. Canfield DE, Thamdrup B (1996) Fate of elemental sulfur in an intertidal sediment. FEMS Microbiol Ecol 19:95–103CrossRefGoogle Scholar
  11. Carreira C, Staal M, Falkoski D, de Vries RP, Middelboe M, Brussaard CPD (2015) Disruption of photoautotrophic intertidal mats by filamentous fungi. Environ Microbiol 17:2910–2921PubMedCrossRefGoogle Scholar
  12. Caumette P (1988) Characterization of Chromatium salexigens sp. nov., a halophilic Chromatiaceae isolated from Mediterranean Salinas. Syst Appl Microbiol 10:284–292CrossRefGoogle Scholar
  13. Caumette P, Baulaigue R, Matheron R (1991) Thiocapsa halophila sp. nov., a new halophilic phototrophic purple sulfur bacterium. Arch Microbiol 155:170–176CrossRefGoogle Scholar
  14. Caumette P, Imhoff JF, Suling J, Matheron R (1997) Chromatium glycolicum sp. nov., a moderately halophilic purple sulfur bacterium that uses glycolate as substrate. Arch Microbiol 167:11–18PubMedCrossRefGoogle Scholar
  15. Caumette P, Guyoneaud R, Duran R, Cravo-Laureau C, Matheron R (2007) Rhodobium pfennigii sp. nov., a phototrophic purple non-sulfur bacterium with unusual bacteriochlorophyll a antennae, isolated from a brackish microbial mat on Rangiroa atoll, French Polynesia. Int J Syst Evol Microbiol 57:1250–1255PubMedCrossRefGoogle Scholar
  16. Cohen Y, Padan E, Shilo M (1975) Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. J Bacteriol 123:855–861PubMedPubMedCentralGoogle Scholar
  17. Crowe SA, Jones C, Katsev S, Magen C, O’Neill AH, Sturm A, Canfield DE, Haffner GD, Mucci A, Sundby B, Fowle DA (2008) Photoferrotrophs thrive in an Archean ocean analogue. Proc Natl Acad Sci 105:15938–15943PubMedPubMedCentralCrossRefGoogle Scholar
  18. Csotonyi J, Swiderski J, Stackebrandt E, Yurkov V (2010) A new environment for aerobic anoxygenic phototrophic bacteria: biological soil crusts. Environ Microbiol Rep 2:651–656PubMedCrossRefGoogle Scholar
  19. D’Amelio ED, Cohen Y, Des Marais DJ (1987) Association of a new type of gliding, filamentous, purple phototrophic bacterium inside bundles of Microcoleus chthonoplastes in hypersaline cyanobacterial mats. Arch Microbiol 147:213–220PubMedCrossRefGoogle Scholar
  20. de Wit R, van Gemerden H (1987a) Oxidation of sulfide to thiosulfate by Microcoleus chthonoplastes. FEMS Microbiol Ecol 45:7–13CrossRefGoogle Scholar
  21. de Wit R, van Gemerden H (1987b) Chemolithotrophic growth of the phototrophic sulfur bacterium Thiocapsa roseopersicina. FEMS Microbiol Ecol 45:117–126CrossRefGoogle Scholar
  22. de Wit R, van Gemerden H (1990) Growth of the phototrophic purple sulfur bacterium Thiocapsa roseopersicina under oxic/anoxic regimens in the light. FEMS Microbiol Ecol 73:69–76CrossRefGoogle Scholar
  23. de Wit R, van Boekel WHM, van Gemerden H (1988) Growth of the cyanobacterium Microcoleus chthonoplastes on sulfide. FEMS Microbiol Ecol 53:203–209CrossRefGoogle Scholar
  24. de Wit R, van den Ende FP, van Gemerden H (1995) Mathematical simulation of the interactions among cyanobacteria, purple sulfur bacteria and chemotrophic sulfur bacteria in microbial mat communities. FEMS Microbiol Ecol 17:117–135CrossRefGoogle Scholar
  25. Dillon JG, Miller S, Bebout B, Hullar M, Pinel N, Stahl DA (2009) Spatial and temporal variability in a stratified hypersaline microbial mat. FEMS Microbiol Ecol 68:46–58PubMedCrossRefGoogle Scholar
  26. Ehrenreich A, Widdel F (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl Environ Microbiol 60:4517–4526PubMedPubMedCentralGoogle Scholar
  27. Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583PubMedCrossRefGoogle Scholar
  28. Fenchel T (1998) Formation of laminated cyanobacterial mats in the absence of benthic fauna. Aquat Microb Ecol 14:235–240CrossRefGoogle Scholar
  29. Fourçans A, García de Oteyza T, Wieland A, Solé A, Diestra E, van Bleijswijk J, Grimalt JO, Kühl M, Esteve I, Muyzer G, Caumette P, Duran R (2004) Characterization of functional bacterial groups in a hypersaline microbial mat community (Salins-de-Giraud, Camargue, France). FEMS Microbiol Ecol 51:55–70PubMedCrossRefGoogle Scholar
  30. Fourçans A, Solé A, Diestra E, Ranchou-Peyruse A, Esteve I (2006) Vertical migration of phototrophic bacterial populations in a hypersaline microbial mat from Salins-de-Giraud (Camargue, France). FEMS Microbiol Ecol 57:367–377PubMedCrossRefGoogle Scholar
  31. Fredriksson C, Malin G, Siddiqui PJA, Bergman B (1998) Aerobic nitrogen fixation is confined to a subset of cells in the non-heterocystous cyanobacterium Symploca PCC 8002. New Phytol 140:531–538CrossRefGoogle Scholar
  32. Gallon JR (1992) Reconciling the incompatible: N2 fixation and O2. New Phytol 122:571–609CrossRefGoogle Scholar
  33. Garcia-Pichel F, Castenholz RW (1991) Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J Phycol 27:395–409CrossRefGoogle Scholar
  34. Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169PubMedPubMedCentralGoogle Scholar
  35. Garcia-Pichel F, Prufert-Bebout L, Muyzer G (1996) Phenotypic and phylogenetic analyses show Microcoleus chthonoplastes to be a cosmopolitan cyanobacterium. Appl Environ Microbiol 62:3284–3291PubMedPubMedCentralGoogle Scholar
  36. Gerdes G, Claes M, Dnajtschik-Piewak K, Riege H, Krumbein WE, Reineck HE (1993) Contribution of microbial mats to sedimentary surface structures. Facies 29:61–74CrossRefGoogle Scholar
  37. Glaeser J, Overmann J (1999) Selective enrichment and characterization of Roseospirillum parvum, gen. nov. and sp. nov., a new purple nonsulfur bacterium with unusual light absorption properties. Arch Microbiol 171:405–416PubMedCrossRefGoogle Scholar
  38. Grant J, Gust G (1987) Prediction of coastal sediment stability from photopigment context of mats of purple sulphur bacteria. Nature 330:244–246CrossRefGoogle Scholar
  39. Guyoneaud R, Matheron R, Baulaigue R, Podeur K, Hirschler A, Caumette P (1996) Anoxygenic phototrophic bacteria in eutrophic coastal lagoons of the French Mediterranean and Atlantic Coasts (Prevost Lagoon, Arcachon Bay, Certes fishponds). Hydrobiologia 329:33–43CrossRefGoogle Scholar
  40. Guyoneaud R, Mouné S, Eatock C, Bothorel V, Hirschler-Rea A, Willison J, Duran R, Liesack W, Herbert R, Matheron R, Caumette P (2002) Characterization of three spiral-shaped purple nonsulfur bacteria isolated from coastal lagoon sediments, saline sulfur springs, and microbial mats: emended description of the genus Roseospira and description of Roseospira marina sp. nov., Roseospira navarrensis sp. nov., and Roseospira thiosulfatophila sp. nov. Arch Microbiol 178:315–324PubMedCrossRefGoogle Scholar
  41. Hamilton TL, Bryant DA, Macalady JL (2016) The role of biology in planetary evolution: cyanobacterial primary production in low-oxygen Proterozoic oceans. Environ Microbiol 18:325–340PubMedCrossRefGoogle Scholar
  42. Heising S, Richter L, Ludwig W, Schink B (1999) Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain. Arch Microbiol 172:116–124PubMedCrossRefGoogle Scholar
  43. Hoehler TM, Bebout BM, Des Marais DJ (2001) The role of microbial mats in the production of reduced gases on the early Earth. Nature 412:324–327PubMedCrossRefGoogle Scholar
  44. Hoehler TM, Albert DB, Alperin MJ, Bebout BM, Martens CS, Des Marais DJ (2002) Comparative ecology of H2 cycling in sedimentary and phototrophic ecosystems. Antonie Van Leeuwenhoek 81:575–585PubMedCrossRefGoogle Scholar
  45. Hoffmann D, Maldonado J, Wojciechowski MF, Garcia-Pichel F (2015) Hydrogen export from intertidal cyanobacterial mats: sources, fluxes and the influence of community composition. Environ Microbiol 17:3738–3753PubMedCrossRefGoogle Scholar
  46. Howarth RW (1979) Pyrite: its rapid formation in a salt marsh and its importance in ecosystem metabolism. Science 203:49–50PubMedCrossRefGoogle Scholar
  47. Imhoff JF (2001) True marine and halophilic anoxygenic phototrophic bacteria. Arch Microbiol 176:243–254PubMedCrossRefGoogle Scholar
  48. Imhoff JF, Petri R, Süling J (1998) Reclassification of species of the spiral-shaped phototrophic purple non-sulfur bacteria of the a-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 48:793–798Google Scholar
  49. Jahnke LL, Turk-Kubo KA, Parenteau MN, Green SJ, Kubo MDY, Vogel M, Summons RE, Des Marais DJ (2014) Molecular and lipid biomarker analysis of a gypsum-hosted endoevaporitic microbial community. Geobiology 12:62–82PubMedCrossRefGoogle Scholar
  50. Jørgensen BB, Cohen Y (1977) Solar Lake (Sinai). 5. The sulfur cycle of the benthic cyanobacterial mats. Limnol Oceanogr 22:657–666Google Scholar
  51. Jørgensen BB, Revsbech NP, Cohen Y (1983) Photosynthesis and structure of benthic microbial mats: micro-electrode and SEM studies of four cyanobacterial communities. Limnol Oceanogr 28:1075–1093CrossRefGoogle Scholar
  52. Kim J, Rees DC (1994) Nitrogenase and biological nitrogen fixation. Biochemistry 33:389–397PubMedCrossRefGoogle Scholar
  53. Klatt JM, Meyer S, Häusler S, Macalady JL, de Beer D, Polerecky L (2016) Structure and function of natural sulphide-oxidizing microbial mats under dynamic input of light and chemical energy. ISME J 10:921–933PubMedCrossRefGoogle Scholar
  54. Koblížek M (2015) Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiol Rev 39:854–870PubMedCrossRefGoogle Scholar
  55. Kohls K, Abed RMM, Polerecky L, Weber M, de Beer D (2010) Halotaxis of cyanobacteria in an intertidal hypersaline microbial mat. Halotaxis of cyanobacteria in an intertidal hypersaline microbial mat. Environ Microbiol 12:567–575PubMedCrossRefGoogle Scholar
  56. Lassen C, Ploug H, Jørgensen BB (1992) A fibre-optic scalar irradiance microsensor - application for spectral light measurements in sediments. FEMS Microbiol Ecol 86:247–254CrossRefGoogle Scholar
  57. Lee K-B, Liu C-T, Anzai Y, Kim H, Aono T, Oyaizu H (2005) The hierarchical system of the ‘Alphaproteobacteria’: description of Hyphomonadaceae fam. nov., Xanthobacteraceae fam. nov. and Erythrobacteraceae fam. nov. Int J Syst Evol Microbiol 55:1907–1919PubMedCrossRefGoogle Scholar
  58. Ley RE, Harris JK, Wilcox J, Spear JR, Millern SR, Bebout BM, Maresca JA, Bryant DA, Sogin ML, Pace NR (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72:3685–3695PubMedPubMedCentralCrossRefGoogle Scholar
  59. Malin G, Walsby AE (1985) Chemotaxis of a cyanobacterium on concentration gradients of carbondioxide, bicarbonate and oxygen. J Gen Microbiol 131:2643–2652Google Scholar
  60. Manske AK, Glaeser J, Kuypers MMM, Overmann J (2005) Physiology and phylogeny of green sulfur bacteria forming a monospecific phototrophic assemblage at a depth of 100 meters in the Black Sea. Appl Environ Microbiol 71:8049–8060PubMedPubMedCentralCrossRefGoogle Scholar
  61. Martinez-Alonso M, van Bleijswijk J, Gaju N, Muyzer G (2005) Diversity of anoxygenic phototrophic sulfur bacteria in the microbial mats of the Ebro delta: a combined morphological and molecular approach. FEMS Microbiol Ecol 52:339–350PubMedCrossRefGoogle Scholar
  62. Meyer KM, Macalady JL, Fulton JM, Kump LR, Schaperdoth I, Freeman KH (2011) Carotenoid biomarkers as an imperfect reflection of the anoxygenic phototrophic community in meromictic Fayetteville Green Lake. Geobiology 9:321–329PubMedCrossRefGoogle Scholar
  63. Nicholson JAM, Stolz JF, Pierson BK (1987) Structure of a microbial mat at Great Sippewissett Marsh, Cape Cod, Massachusetts. FEMS Microbiol Ecol 45:343–364CrossRefGoogle Scholar
  64. Nishimura Y, Muroga Y, Saito S, Shiba T, Takamiya K-I, Shioi Y (1994) DNA relatedness and chemotaxonomic feature of aerobic bacteriochlorophyll-containing bacteria isolated from coasts of Australia. J Gen Appl Microbiol 40:287–296CrossRefGoogle Scholar
  65. Olson JB, Litaker RW, Paerl HW (1999) Ubiquity of heterotrophic diazotrophs in marine microbial mats. Aquat Microb Ecol 19:29–36CrossRefGoogle Scholar
  66. Omoregie EO, Crumbliss LL, Bebout BM, Zehr JP (2004) Determination of nitrogen-fixing phylotypes in Lyngbya sp. and Microcoleus chthonoplastes cyanobacterial mats from Guerrero Negro, Baja California, Mexico. Appl Environ Microbiol 70:2119–2128PubMedPubMedCentralCrossRefGoogle Scholar
  67. Overmann J, Garcia-Pichel F (2006) The phototrophic way of life. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH (eds) The prokaryotes, vol 2. Springer, Heidelberg, pp 32–85Google Scholar
  68. Padan E (1979) Facultative anoxygenic photosynthesis in cyanobacteria. Annu Rev Plant Physiol 30:27–40CrossRefGoogle Scholar
  69. Pearson HW, Howsley R, Kjeldsen CK, Walsby AE (1979) Aerobic nitrogenase activity associated with a non-heterocystous filamentous cyanobacterium. FEMS Microbiol Lett 5:163–169CrossRefGoogle Scholar
  70. Pierson BK, Oesterle A, Murphy GL (1987) Pigments, light penetration, and photosynthetic activity in the multi-layered microbial mats of Great Sippewissett salt marsh, Massachusetts. FEMS Microbiol Ecol 45:365–376CrossRefGoogle Scholar
  71. Pierson BK, Parenteau MN, Griffin BM (1999) Phototrophs in high-iron-concentration microbial mats: physiological ecology of phototrophs in an iron-depositing hot spring. Appl Environ Microbiol 65:5474–5483PubMedPubMedCentralGoogle Scholar
  72. Polerecky L, Bachar A, Schoon R, Grinstein M, Jørgensen BB, de Beer D, Jonkers HM (2007) Contribution of Chloroflexus respiration to oxygen cycling in a hypersaline microbial mat from Lake Chiprana, Spain. Environ Microbiol 9:2007–2024PubMedCrossRefGoogle Scholar
  73. Potts M, Krumbein WE, Metzger J (1978) Nitrogen fixation rates in anaerobic sediments determined by acetylene reduction, a new 15N field assay, and simultaneous total N 15N determination. In: Krumbein WE (ed) Environmental biogeochemistry and geomicrobiology vol 3: methods, metals and assessment. Ann Arbor Science, Ann Arbor Michigan, pp 753–769Google Scholar
  74. Pringault O, Garcia-Pichel F (2004) Hydrotaxis of cyanobacteria in desert crusts. Microbial Ecol 47:366–373. Appl Environ Microbiol 66:1038–1049Google Scholar
  75. Pringault O, Epping E, Guyoneaud R, Khalili A, Kühl M (1999) Dynamics of anoxygenic photosynthesis in an experimental green sulphur bacteria biofilm. Environ Microbiol 1:295–305PubMedCrossRefGoogle Scholar
  76. Rai AN, Söderbäck E, Bergman B (2000) Cyanobacterium-plant symbioses. New Phytol 147:449–481CrossRefGoogle Scholar
  77. Ramsing NB, Ferris MJ, Ward DM (2000) Highly ordered vertical structure of Synechococcus populations within the one-millimeter-thick photic zone of a hot spring cyanobacterial mat. Appl Environ Microbiol 66:1038–1049Google Scholar
  78. Ranchou-Peyruse A, Moppert X, Hourcade E, Hernandez G, Caumette P, Guyoneaud R (2004) Characterization of brackish anaerobic bacteria involved in hydrocarbon degradation: a combination of molecular and culture-based approaches. Ophelia 58:255–262CrossRefGoogle Scholar
  79. Ranchou-Peyruse A, Herbert R, Caumette P, Guyoneaud R (2006) Comparison of cultivation-dependent and molecular methods for studying the diversity of anoxygenic purple phototrophs in sediments of an eutrophic brackish lagoon. Environ Microbiol 8:1590–1599PubMedCrossRefGoogle Scholar
  80. Revsbech NP, Jørgensen BB, Blackburn TH, Cohen Y (1983) Microelectrode studies of the photosynthesis and O2, H2S and pH profiles of a microbial mat. Limnol Oceanogr 28:1062–1074CrossRefGoogle Scholar
  81. Richardson LL, Castenholz RW (1987) Diel vertical movements of the cyanobacterium Oscillatoria terebriformis in a sulfide-rich hot spring microbial mat. Appl Environ Microbiol 53:2142–2150PubMedPubMedCentralGoogle Scholar
  82. Richardson LL, Castenholz RW (1989) Chemokinetic motility responses of the cyanobacterium Oscillatoria terebriformis. Appl Environ Microbiol 55:261–263PubMedPubMedCentralGoogle Scholar
  83. Rippka R, Waterbury JB (1977) The synthesis of nitrogenase by non-heterocystous cyanobacteria. FEMS Microbiol Lett 2:83–86CrossRefGoogle Scholar
  84. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  85. Risatti JB, Capman WC, Stahl DA (1994) Community structure of a microbial mat: the phylogenetic dimension. Proc Natl Acad Sci U S A 91:10173–10177PubMedPubMedCentralCrossRefGoogle Scholar
  86. Schaub BEM, van Gemerden H (1994) Simultaneous phototrophic and chemotrophic growth in the purple sulfur bacterium Thiocapsa roseopersicina M1. FEMS Microbiol Ecol 13:185–195CrossRefGoogle Scholar
  87. Severin I, Stal LJ (2010) Diazotrophic microbial mats. In: Seckbach J, Oren A (eds) Microbial mats. Modern and ancient microorganisms in stratified systems. Springer, Heidelberg, pp 321–339Google Scholar
  88. Severin I, Acinas SG, Stal LJ (2010) Diversity of nitrogen-fixing bacteria in cyanobacterial mats. FEMS Microbiol Ecol 73:514–525PubMedGoogle Scholar
  89. Shiba T (1991) Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a. Syst Appl Microbiol 14:140–145CrossRefGoogle Scholar
  90. Shiba T, Simidu U, Taga N (1979) Distribution of aerobic bacteria which contain bacteriochlorophyll a. Appl Environ Microbiol 38:43–45PubMedPubMedCentralGoogle Scholar
  91. Siegesmund M, Johansen JR, Karsten U, Friedl T (2008) Coleofasciculus gen. nov. (Cyanobacteria): morphological and molecular criteria for revision of the genus Microcoleus Gomont. J Phycol 44:1572–1585PubMedCrossRefGoogle Scholar
  92. Sigalevich P, Baev MV, Teske A, Cohen Y (2000) Sulfate reduction and possible aerobic metabolism of the sulfate-reducing bacterium Desulfovibrio oxyclinae in a chemostat coculture with Marinobacter sp. strain MB under exposure to increasing oxygen concentrations. Appl Environ Microbiol 66:5013–5018PubMedPubMedCentralCrossRefGoogle Scholar
  93. Stal LJ (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol 131:1–32CrossRefGoogle Scholar
  94. Stal LJ (2001) Coastal microbial mats: the physiology of a small-scale ecosystem. S Afr J Bot 67:399–410CrossRefGoogle Scholar
  95. Stal LJ (2012) Microbial mats and stromatolites. In: Whitton BA (ed) The ecology of cyanobacteria. Springer, Dordrecht, pp 61–120Google Scholar
  96. Stal LJ, Heyer H (1987) Dark anaerobic nitrogen fixation (acetylene reduction) in the cyanobacterium Oscillatoria sp. FEMS Microbiol Ecol 45:227–232CrossRefGoogle Scholar
  97. Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS Microbiol Rev 21:179–211CrossRefGoogle Scholar
  98. Stal LJ, van Gemerden H, Krumbein WE (1985) Structure and development of a benthic marine microbial mat. FEMS Microbiol Ecol 31:111–125CrossRefGoogle Scholar
  99. Steinmetz MA, Fischer U (1982) Cytochromes, rubredoxin and sulfur metabolism of the non-thiosulfate-utilizing green sulfur bacterium Pelodictyon luteolum. Arch Microbiol 132:204–210CrossRefGoogle Scholar
  100. Steppe TF, Olson JB, Paerl HW, Litaker RW, Belnap J (1996) Consortial N2 fixation: a strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol Ecol 21:149–156CrossRefGoogle Scholar
  101. Steudel R, Holdt G, Visscher PT, van Gemerden H (1990) Search for polythionates in cultures of Chromatium vinosum after sulfide incubation. Arch Microbiol 153:432–437CrossRefGoogle Scholar
  102. Tang K-H, Feng X, Tang YJ, Blankenship RE (2009) Carbohydrate metabolism and carbon fixation in Roseobacter denitrificans OCh114. PLoS One 4(10):e7233PubMedPubMedCentralCrossRefGoogle Scholar
  103. Then J, Trüper HG (1981) The role of thiosulfate in sulfur metabolism of Rhodopseudomonas globiformis. Arch Microbiol 130:143–146CrossRefGoogle Scholar
  104. Thiel V, Tank M, Neulinger SC, Gehrmann L, Dorador C, Imhoff JF (2010) Unique communities of anoxygenic phototrophic bacteria in saline lakes of Salar de Atacama (Chile): evidence for a new phylogenetic lineage of phototrophic Gammaproteobacteria from pufLM gene analyses. FEMS Microbiol Ecol 74:510–522PubMedCrossRefGoogle Scholar
  105. Urmeneta J, Alcoba Ó, Razquín E, Tarroja E, Navarrete A, Guerrero R (1998) Oxygenic photosynthesis and respiratory activity in microbial mats of the Ebro delta, Spain, by oxygen exchange method. Curr Microbiol 37:151–155PubMedCrossRefGoogle Scholar
  106. van der Meer MTJ, Schouten S, Bateson MM, Nübel U, Wieland A, Kühl M, De Leeuw JW, Sinninghe Damste JS, Ward DM (2005) Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline siliceous hot spring microbial mats from Yellowstone national park. Appl Environ Microbiol 71:3978–3986PubMedPubMedCentralCrossRefGoogle Scholar
  107. van Gemerden H (1984) The sulfide affinity of phototrophic bacteria in relation to the location of elemental sulfur. Arch Microbiol 139:289–294CrossRefGoogle Scholar
  108. van Gemerden H (1993) Microbial mats: a joint venture. Mar Geol 113:3–25CrossRefGoogle Scholar
  109. van Gemerden H, de Wit R, Tughan CS, Herbert RA (1989a) Development of mass blooms of Thiocapsa roseopersicina on sheltered beaches on the Orkney Islands. FEMS Microbiol Lett 62:111–118CrossRefGoogle Scholar
  110. van Gemerden H, Tughan CS, de Wit R, Herbert RA (1989b) Laminated microbial ecosystems on sheltered beaches in Scapa Flow, Orkney Islands. FEMS Microbiol Ecol 62:87–102CrossRefGoogle Scholar
  111. Villanueva L, del Campo J, Guerrero R, Geyer R (2010) Intact phospholipid and quinone biomarkers to assess microbial diversity and redox state in microbial mats. Microb Ecol 60:226–238PubMedCrossRefGoogle Scholar
  112. Villbrandt M, Stal LJ, Krumbein WE (1990) Interactions between nitrogen fixation and oxygenic photosynthesis in a marine cyanobacterial mat. FEMS Microbiol Ecol 74:59–72CrossRefGoogle Scholar
  113. Visscher PT, van Gemerden H (1991) Production and consumption of dimethylsulfoniopropionate in marine microbial mats. Appl Environ Microbiol 57:3237–3242PubMedPubMedCentralGoogle Scholar
  114. Visscher PT, van Gemerden H (1993) Sulfur cycling in laminated marine microbial ecosystems. In: Oremland RS (ed) Biogeochemistry of global change: radiatively active trace gases. Chapman and Hall, New York, pp 672–690CrossRefGoogle Scholar
  115. Visscher PT, Nijburg JW, van Gemerden H (1990) Polysulfide utilization by Thiocapsa roseopersicina. Arch Microbiol 155:75–81CrossRefGoogle Scholar
  116. Visscher PT, Prins RA, van Gemerden H (1992) Rates of sulfate reduction and thiosulfate consumption in a marine microbial mat. FEMS Microbiol Ecol 86:283–293CrossRefGoogle Scholar
  117. Watermann F, Hillebrand H, Gerdes G, Krumbein WE, Sommer U (1999) Competition between benthic cyanobacteria and diatoms as influenced by different grain sizes and temperatures. Mar Ecol Prog Ser 187:77–87CrossRefGoogle Scholar
  118. Wieland A, Kühl M, McGowan L, Fourçans A, Duran R, Caumette P, Garcia de Oteyza T, Grimalt JO, Solé A, Diestra E, Herbert RA (2003) Microbial mats on the Orkney Islands revisited: microenvironment and microbial community composition. Microb Ecol 46:371–390PubMedCrossRefGoogle Scholar
  119. Wieland A, Zopfi J, Benthien M, Kühl M (2005) Biogeochemistry of an iron-rich hypersaline microbial mat (Camargue, France). Microb Ecol 49:34–49PubMedCrossRefGoogle Scholar
  120. Yallop ML, de Winder B, Paterson DM, Stal LJ (1994) Comparative structure, primary production and biogenic stabilization of cohesive and non-cohesive marine sediments inhabited by microphytobenthos. Estuar Coast Shelf Sci 39:565–582CrossRefGoogle Scholar
  121. Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724PubMedPubMedCentralGoogle Scholar
  122. Yurkov V, Gorlenko VM (1992) Ecophysiological peculiarities of phototrophic microbial communities of Bolsherechensky thermal springs. Microbiology 61:115–122Google Scholar
  123. Yurkov VV, van Gemerden H (1993) Abundance and salt tolerance of obligately aerobic, phototrophic bacteria in a marine microbial mat. Neth J Sea Res 31:57–62CrossRefGoogle Scholar
  124. Yurkov V, Krasilnikova EN, Gorlenko VM (1994) Thiosulfate metabolism in aerobic bacteriochlorophyll-a containing bacteria. Microbiology 63:181–188Google Scholar
  125. Zehr JP, Mellon M, Braun S, Litaker W, Steppe T, Paerl HW (1995) Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl Environ Microbiol 61:2527–2532PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Lucas J. Stal
    • 1
    • 2
  • Henk Bolhuis
    • 1
  • Mariana Silvia Cretoiu
    • 1
  1. 1.Department of Marine Microbiology and BiogeochemistryRoyal Netherlands Institute for Sea Research and Utrecht UniversityYersekeThe Netherlands
  2. 2.Department of Aquatic MicrobiologyUniversity of AmsterdamAmsterdamThe Netherlands

Personalised recommendations