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Amino acid-assimilating phototrophic heliobacteria from soda lake environments: Heliorestis acidaminivorans sp. nov. and ‘Candidatus Heliomonas lunata’

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Abstract

Two novel taxa of heliobacteria, Heliorestis acidaminivorans sp. nov. strain HR10BT and ‘Candidatus Heliomonas lunata’ strain SLH, were cultured from shoreline sediments/soil of Lake El Hamra (Egypt) and lake water/benthic sediments of Soap Lake (USA), respectively; both are highly alkaline soda lakes. Cells of strain HR10B were straight rods, while cells of strain SLH were curved rods. Both organisms were obligate anaerobes, produced bacteriochlorophyll g, and lacked intracytoplasmic photosynthetic membrane systems. Although the absorption spectrum of strain HR10B was typical of other heliobacteria, that of strain SLH showed unusually strong absorbance of the OH-chlorophyll a component. Major carotenoids of both organisms were OH-diaponeurosporene glucosyl esters, as in other alkaliphilic heliobacteria, and both displayed an alkaliphilic and mesophilic phenotype. Strain HR10B was remarkable among heliobacteria in its capacity to photoassimilate a number of carbon sources, including several amino acids. Nitrogenase activity was observed in strain HR10B, but not in strain SLH. The 16S ribosomal RNA gene tree placed strain HR10B within the genus Heliorestis, but distinct from other described species. By contrast, strain SLH was phylogenetically more closely related to neutrophilic heliobacteria and is the first alkaliphilic heliobacterium known outside of the genus Heliorestis.

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References

  • Asao M, Madigan MT (2010) Taxonomy, phylogeny, and ecology of the heliobacteria. Photosynth Res 104:103–111

    Article  PubMed  CAS  Google Scholar 

  • Asao M, Jung DO, Achenbach LA, Madigan MT (2006) Heliorestis convoluta sp. nov., a coiled, alkaliphilic heliobacterium from the Wadi El Natroun, Egypt. Extremophiles 10:403–410

    Article  PubMed  CAS  Google Scholar 

  • Asao M, Takaichi S, Madigan MT (2007) Thiocapsa imhoffii, sp. nov., an alkaliphilic purple sulfur bacterium of the family Chromatiaceae from Soap Lake, Washington (USA). Arch Microbiol 188:665–675

    Article  PubMed  CAS  Google Scholar 

  • Asao M, Pinkart HC, Madigan MT (2011) Diversity of extremophilic purple phototrophic bacteria in Soap Lake, a Central Washington (USA) Soda Lake. Environ Microbiol 13:2146–2157

    Article  PubMed  CAS  Google Scholar 

  • Brockmann H, Lipinski A (1983) Bacteriochlorophyll g. A new bacteriochlorophyll from Heliobacterium chlorum. Arch Microbiol 136:17–19

    Article  CAS  Google Scholar 

  • Bryantseva IA, Gorlenko VM, Kompantseva EI, Achenbach LA, Madigan MT (1999) Heliorestis daurensis, gen. nov. sp. nov., an alkaliphilic rod-to-coiled-shaped phototrophic heliobacterium from a Siberian soda lake. Arch Microbiol 172:167–174

    Article  PubMed  CAS  Google Scholar 

  • Bryantseva IA, Gorlenko VM, Kompantseva EI, Tourova TP, Kuznetsov BB, Lysenko AM, Bykova SA, Galchenko VF, Osipov GA (2000a) Heliobacterium sulfidophilum sp. nov. and Heliobacterium undosum sp. nov.: sulfide-oxidizing heliobacteria from thermal sulfidic springs. Microbiology (English translation of Mikrobiologia) 69:325–334

    CAS  Google Scholar 

  • Bryantseva IA, Gorlenko VM, Tourova TP, Kuznetsov BB, Osipov GA (2000b) Alkaliphilic heliobacterium Heliorestis baculata sp. nov. and emended description of the genus Heliorestis. Arch Microbiol 174:283–291

    Article  PubMed  CAS  Google Scholar 

  • Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM, Tiedje JM (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucl Acids Res 31:442–443

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1989) PHYLIP-Phylogeny inference package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Gest H (1994) Discovery of the heliobacteria. Photosynth Res 41:17–21

    Article  CAS  Google Scholar 

  • Grant WD, Mwatha WE, Jones BE (1990) Alkaliphiles: ecology, diversity and applications. FEMS Microbiol Rev 75:255–270

    Article  CAS  Google Scholar 

  • Imhoff JF (2001) True marine and halophilic anoxygenic phototrophic bacteria. Arch Microbiol 176:243–254

    Article  PubMed  CAS  Google Scholar 

  • Imhoff JF (2006) The Chromatiaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E (eds) The prokaryotes, 3rd edn. Springer, New York, pp 846–873

    Chapter  Google Scholar 

  • Imhoff JF, Hashwa F, Trüper HG (1978) Isolation of extremely halophilic phototrophic bacteria from the alkaline Wadi Natrun, Egypt. Arch Hydrobiol 84:381–388

    Google Scholar 

  • Imhoff JF, Sahl HG, Soliman GSH, Trüper HG (1979) TheWadi Natrun: chemical composition and microbial mass developments in alkaline brines of eutrophic desert lakes. Geomicrobiol J 1:219–234

    Article  CAS  Google Scholar 

  • Jones BE, Grant WD, Duckworth AW, Owenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2:191–200

    Article  PubMed  CAS  Google Scholar 

  • Kimble LK, Madigan MT (1992) Nitrogen fixation and nitrogen metabolism in heliobacteria. Arch Microbiol 158:155–161

    Article  CAS  Google Scholar 

  • Kimble LK, Stevenson AK, Madigan MT (1994) Chemotrophic growth of heliobacteria in darkness. FEMS Microbiol Lett 115:51–56

    Article  PubMed  CAS  Google Scholar 

  • Kimble LK, Mandelco L, Woese CR, Madigan MT (1995) Heliobacterium modesticaldum, sp. nov., a thermophilic heliobacterium of hot springs and volcanic soils. Arch Microbiol 163:259–267

    Article  CAS  Google Scholar 

  • Kobayashi M, van de Meent EJ, Erkelens C, Amesz J, Ikegami I, Watanabe T (1991) Bacteriochlorophyll g epimer as a possible reaction center component of heliobacteria. Biochim Biophys Acta 1057:89–96

    Article  CAS  Google Scholar 

  • Madigan MT (1988) Microbiology, physiology, and ecology of phototrophic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 39–111

    Google Scholar 

  • Madigan MT (1995) Microbiology of nitrogen fixation by anoxygenic photosynthetic bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordorecht, pp 915–928

    Google Scholar 

  • Madigan MT (2001) Heliobacteriaceae. In: Boone D, Castenholtz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, Berlin, pp 625–630

    Google Scholar 

  • Madigan MT (2003) Anoxygenic phototrophic bacteria from extreme environments. Photosynth Res 76:157–171

    Article  PubMed  CAS  Google Scholar 

  • Madigan MT, Jung DO (2009) An overview of purple bacteria: systematics, physiology, and habitats. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The purple phototrophic bacteria. Springer, Dordrecht, pp 1–15

    Chapter  Google Scholar 

  • Madigan MT, Ormerod JG (1995) Taxonomy, physiology, and ecology of heliobacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic, Dordrecht, pp 17–30

    Google Scholar 

  • Miller KR, Jacob JS, Smith U, Kolaczkowski S, Bowman MK (1986) Heliobacterium chlorum: cell organization and structure. Arch Microbiol 146:111–114

    Article  PubMed  CAS  Google Scholar 

  • Murray RG, Stackebrandt E (1995) Taxonomic note: implementation of the provisional status Candidatus for incompletely described prokaryotes. Int J Syst Bacteriol 45:186–187

    Article  PubMed  CAS  Google Scholar 

  • Neerken S, Amesz J (2001) The antenna reaction center complex of heliobacteria: composition, energy conversion and electron transfer. Biochim Biophys Acta 1507:278–290

    Article  PubMed  CAS  Google Scholar 

  • Oremland RS, Miller LG (1993) Biogeochemistry of natural gases in three alkaline permanently stratified meromictic lakes. The Future of Energy Gases, USGS Paper 1570:439–452

    Google Scholar 

  • Ormerod JG, Kimble LK, Nesbakken T, Torgersen YA, Woese CR, Madigan MT (1996) Heliophilum fasciatum gen. nov. sp. nov. and Heliobacterium gestii sp. nov.: endospore-forming heliobacteria from rice field soils. Arch Microbiol 165:226–234

    Article  PubMed  CAS  Google Scholar 

  • Pfennig N (1967) Photosynthetic bacteria. Ann Rev Microbiol 21:285–324

    Article  CAS  Google Scholar 

  • Pfennig N (1978) General physiology and ecology of photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 3–18

    Google Scholar 

  • Pickett MW, Williamson MP, Kelly DJ (1994) An enzyme and 13C-NMR study of carbon metabolism in heliobacteria. Photosynth Res 41:75–88

    Article  CAS  Google Scholar 

  • Rice CA, Tuttle ML, Briggs PH (1988) Sulfur speciation, sulfur isotopy, and elemental analyses of water-column, pore water, and sediment samples from Soap Lake, Washington. US Geological Survey Open-file report no. 88-22:1–24

  • Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Mirobiol Rev 25:39–67

    Article  Google Scholar 

  • Sattley WM et al (2008) The genome of Heliobacterium modesticaldum, a phototrophic representative of the Firmicutes containing the simplest photosynthetic apparatus. J Bacteriol 190:4687–4696

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Foti M, Pinkart HC, Muyzer G (2007) Sulfur-oxidizing bacteria in Soap Lake (Washington State), a meromictic, haloalkaline lake with an unprecedented high sulfide content. Appl Environ Microbiol 73:451–455

    Article  PubMed  CAS  Google Scholar 

  • Stevenson AK, Kimble LK, Woese CR, Madigan MT (1997) Characterization of new phototrophic heliobacteria and their habitats. Photosynth Res 53:1–12

    Article  CAS  Google Scholar 

  • Taher AG (1999) Inland saline lakes of Wadi El Natrun depression, Egypt. Int J Salt Lake Res 8:149–169

    Google Scholar 

  • Takaichi S, Inoue K, Akaike M, Kobayashi M, Oh-oka H, Madigan MT (1997) The major carotenoid in all known species of heliobacteria is the C30 carotenoid 4,4′-diaponeurosporene, not neurosporene. Arch Microbiol 168:277–281

    Article  PubMed  CAS  Google Scholar 

  • Takaichi S, Oh-oka H, Maoka T, Jung DO, Madigan MT (2003) Novel carotenoid glucoside esters from alkaliphilic heliobacteria. Arch Microbiol 179:95–100

    PubMed  CAS  Google Scholar 

  • Wahlund TM, Woese CR, Castenholz RW, Madigan MT (1991) A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch Microbiol 156:81–90

    Article  CAS  Google Scholar 

  • Walker KF (1974) The stability of meromictic lakes in central Washington. Limnol Oceanogr 19:209–222

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the US National Science Foundation Grants 0237576 and 0950550. We thank Dr. Holly Pinkart, Central Washington University, and Deborah O. Jung, Southern Illinois University Carbondale, for help in sampling at Soap Lake. We thank Steven J. Schmitt, SIU Micro-Imaging and Analysis Center, for electron microscopy, and Prof. Aharon Oren, Hebrew University Jerusalem, for nomenclatural advice.

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Correspondence to Michael T. Madigan.

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Communicated by F. Robb.

This paper is dedicated to the memory of Howard Gest, co-discoverer of the heliobacteria.

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Asao, M., Takaichi, S. & Madigan, M.T. Amino acid-assimilating phototrophic heliobacteria from soda lake environments: Heliorestis acidaminivorans sp. nov. and ‘Candidatus Heliomonas lunata’. Extremophiles 16, 585–595 (2012). https://doi.org/10.1007/s00792-012-0458-8

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