Heliobacteria

Abstract

Heliobacteria are the most recently discovered of the anoxygenic phototrophic bacteria. Heliobacteria contain bacteriochlorophyll g, a pigment unique to species of this group, and synthesise the simplest photosynthetic complexes of all known phototrophs. Also, unlike all other phototrophs, heliobacteria produce endospores but cannot grow autotrophically. Four genera of heliobacteria are known. Species of Heliobacterium, Heliobacillus and Heliophilum grow best at neutral pH, whereas species of Heliorestis are alkaliphilic. Heliobacterium, Heliobacillus and Heliophilum species form one phylogenetic clade whereas Heliorestis species form a second within the phylum Firmicutes of the domain Bacteria. Heliobacteria have a unique ecology, being primarily terrestrial rather than aquatic, and some species may have evolved a mutualistic relationship with rice plants. The genome sequence of the thermophile Heliobacterium modesticaldum supports the hypothesis that heliobacteria are minimalist phototrophs, and because of this, heliobacteria may have played a pivotal role in the evolution of phototrophic bacteria.

Key Concepts:

  • Heliobacteria are unlike all known anoxygenic phototrophic bacteria because of their unique bacteriochlorophyll, Gram‐positive phylogeny, and primarily soil habitat.

  • Heliobacteria employ the simplest of all photosynthetic energy‐generating systems and thus their study may yield important clues to when and how photosynthesis evolved.

  • In addition to being phototrophic, heliobacteria are strong nitrogen‐fixing bacteria and possibly associate with plants such as rice in a type of symbiotic association.

Keywords: anoxygenic phototrophic bacteria; heliobacteria; bacteriochlorophyll g

Figure 1.

Enrichment cultures for anoxygenic phototrophic bacteria using a paddy soil sample. (a) If the enrichment was not pasteurised (heat‐treated at 80°C for 15 min) (tube 1), the sample yielded purple nonsulfur bacteria (purple‐red turbidity), in this case, Rhodopseudomonas palustris, a common purple bacterium. However, if a duplicate enrichment was pasteurised (tube 2), the purple bacteria in the sample are killed and heliobacteria (green turbidity) develop, presumably from the germination of heliobacterial endospores. (b) Phase‐contrast photomicrograph of a pasteurised enrichment culture. Note spores and sporulating cells (arrows).

Figure 2.

The thermophilic heliobacterium, Heliobacterium modesticaldum. (a) Thin section transmission electron micrograph of cells of Heliobacterium modesticaldum. (b) Scanning electron micrograph of cells. Note flagella scattered in the preparation. Note the absence of an outer membrane and any type of internal photosynthetic membranes or chlorosomes. Cells of Heliobacterium modesticaldum are approximately 1 μm wide.

Figure 3.

Heliorestis convoluta. (a) Phase‐contrast micrograph of long cell coils. (b) Scanning electron micrograph of a short coil of cells. Coils form from ring‐shaped cells that remain connected after cell division. Cells of Heliorestis convoluta are approximately 0.6 μm wide.

Figure 4.

Phylogenetic tree of the family Heliobacteriaceae based on 16S rRNA gene sequences of 1261 nucleotide positions. The tree was computed using PHYLIP version 3.66 (Felsenstein, ). Alignment was converted to a distance matrix using F84 algorithm (transition/transversion ratio=2.0, empirical base frequencies) in the program DNADIST. The tree was based on neighbour‐joining method using the program NEIGHBOR. The tree was rooted using Escherichia coli (Gammaproteobacteria) as an outgroup. All sequences have been deposited in GenBank as follows: E. coli (J01859), Bacillus subtilis (AJ276351), Desulfitobacterium dehalogenans (L28946), Clostridium pasteurianum (M23930), Heliorestis baculata (AF249680), Heliorestis convoluta (DQ266255), Heliophilum fasciatum (L36197), Heliobacterium modesticaldum (U14559), Heliobacterium chlorum (M11212) and Heliobacillus mobilis (U14560).

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References

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

Asao M and Madigan MT (2009) The family Heliobacteriaceae. In: Whitman WB (ed.) Bergey's Manual of Systematic Bacteriology, 2nd edn, pp. 913–920. New York: Springer.

Asao M and Madigan MT (2010) Taxonomy, phylogeny, and ecology of the heliobacteria. Photosynthesis Research. In press.

Beer‐Romero P, Favinger JL and Gest H (1988) Distinctive properties of bacilliform photosynthetic heliobacteria. FEMS Microbiology Letters 49: 451–454.

Beer‐Romero P and Gest H (1987) Heliobacillus mobilis, a peritrichously flagellated anoxyphototroph containing bacteriochlorophyll g. FEMS Microbiology Letters 41: 109–114.

Blankenship RE (2002) Molecular Mechanisms of Photosynthesis. Oxford, UK: Blackwell Scientific.

Blankenship RE, Madigan MT and Bauer CE (eds) (1995) Anoxygenic Photosynthetic Bacteria. Dordrecht, The Netherlands: Kluwer Academic Publication.

Brockmann H and Lapinski A (1983) Bacteriochlorophyll g. A new bacteriochlorophyll from Heliobacterium chlorum. Archives of Microbiology 136: 17–19.

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

Gest H (1994) Discovery of heliobacteria. Photosynthesis Research 41: 17–21.

Gest H and Favinger JL (1983) Heliobacterium chlorum, an anoxygenic brownish‐green photosynthetic bacterium containing a “new” form of bacteriochlrophyll. Archives of Microbiology 136: 11–16.

Kimble LK and Madigan MT (1992) N2 fixation and nitrogen metabolism in heliobacteria. Archives of Microbiology 158: 155–161.

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

Kimble LK, Stevenson AK and Madigan MT (1994) Chemotrophic growth of heliobacteria in darkness. FEMS Microbiology Letters 115: 51–56.

Kimble‐Long LK and Madigan MT (2001) Molecular evidence that the capacity for endosporulation is universal among phototrophic heliobacteria. FEMS Microbiology Letters 199: 191–195.

Kimble‐Long LK and Madigan MT (2002) Irradiance effects on growth and pigment content of heliobacteria, purple and green bacteria. Photosynthetica 40: 629–632.

Madigan MT (1992) The family Heliobacteriaceae. In: Balows A, Trüper HG, Dworkin M, Harder W and Schleifer K‐H (eds) The Prokaryotes, 2nd edn, pp. 1981–1992. Berlin: Springer.

Madigan MT (2006) The family Heliobacteriaceae. Prokaryotes 4: 951–964.

Madigan MT, Martinko JM, Dunlap PV and Clark DP (2009) Brock Biology of Microorganisms, 12th edn. San Francisco, CA: Benjamin‐Cummings.

Madigan MT and Ormerod JG (1995) Taxonomy, physiology, and ecology of heliobacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp. 17–30. Dordrecht, The Netherlands: Kluwer Academic Publishers.

Ormerod JG, Kimble LK, Nesbakken T et al. (1996) Heliophilum fasciatum gen. nov. sp. nov. and Heliobacterium gestii sp. nov.: endospore‐forming heliobacteria from rice field soils. Archives of Microbiology 165: 226–234.

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

Raymond J, Zhaxybayeva O, Gogarten JP and Blankenship RE (2003) Evolution of photosynthetic prokaryotes: a maximum‐likelihood mapping approach. Philosophical Transactions of the Royal Society of London, Series B 358: 223–230.

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

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

Takaichi S, Inoue K, Akaike M et al. (1997) The major carotenoid in all known species of heliobacteria is the C30 carotenoid 4,4′‐diaponeurosporene, not neurosporene. Archives of Microbiology 168: 277–281.

Takaichi S, Oh‐oka H, Maoka T, Jung DO and Madigan MT (2003) Novel carotenoid glucoside esters from alkaliphilic heliobacteria. Archives of Microbiology 179: 95–100.

Woese CR, Debrunner‐Vossbrinck BA, Oyaizu H, Stackebrandt E and Ludwig W (1985) Gram‐positive bacteria: possible photosynthetic ancestry. Science 229: 762–765.

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Asao, Marie, and Madigan, Michael T(Sep 2010) Heliobacteria. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021935]