Abstract
Photosynthesis first emerged in prokaryotes over three billion years ago and represents one of the most fundamental biological processes on Earth. So far, species capable of performing (bacterio)chlorophyll-based phototrophy have been reported in seven bacterial phyla, i.e., Cyanobacteria, Proteobacteria, Chlorobi, Chloroflexi, Firmicutes, Acidobacteria, and Gemmatimonadetes. Here we review the discovery, physiology, genomic characteristics, environmental distribution, and possible evolutionary origin of the bacterium Gemmatimonas phototrophica strain AP64, so far the only phototrophic member of the phylum Gemmatimonadetes. This organism was isolated from a freshwater lake in the Gobi Desert, North China in 2011. It contains fully functional type-2 photosynthetic reaction centers, but they seem to only serve as an auxiliary energy source. Its photosynthesis genes are located in a 42.3 kb long photosynthesis gene cluster which appear to originate from an ancient horizontal gene transfer from a purple phototrophic bacterium. A survey of biomarker genes of phototrophic Gemmatimonadetes bacteria (PGB) in public environmental genomics databases suggests that PGB are widely distributed in diverse environments, including air, river waters/sediment, estuarine waters, lake waters, biofilms, plant surfaces, intertidal sediments, soils, springs, and wastewater treatment plants, but none from marine waters or sediment. PGB make up roughly 0.4–11.9 % of whole phototrophic microbial communities in these habitats. The discovery of PGB presents a strong evidence that genes for anoxygenic phototrophy can be transferred between distant bacterial phyla, providing new insights into the evolution of bacterial photosynthesis.
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Abbreviations
- BChl:
-
Bacteriochlorophyll
- PGB:
-
Phototrophic Gemmatimonadetes bacteria
- PGC:
-
Photosynthesis gene cluster
References
Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH (2013) Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 31(6):533–538
Boldareva-Nuianzina EN, Blahova Z, Sobotka R, Koblížek M (2013) Distribution and origin of oxygen-dependent and oxygen-independent forms of Mg-protoporphyrin monomethylester cyclase among phototrophic proteobacteria. Appl Environ Microbiol 79(8):2596–2604
Breidenbach B, Pump J, Dumont MG (2015) Microbial community structure in the rhizosphere of rice plants. Front Microbiol 6:1537
Bryant DA, Costas AMG, Maresca JA, Chew AGM, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus chloracidobacterium thermophilum: An aerobic phototrophic acidobacterium. Science 317(5837):523–526
Canfield DE, Rosing MT, Bjerrum C (2006) Early anaerobic metabolisms. Philos Trans R Soc B 361(1474):1819–1834
Canniffe DP, Jackson PJ, Hollingshead S, Dickman MJ, Hunter CN (2013) Identification of an 8-vinyl reductase involved in bacteriochlorophyll biosynthesis in Rhodobacter sphaeroides and evidence for the existence of a third distinct class of the enzyme. Biochem J 450(2):397–405
Cardona T (2016) Origin of bacteriochlorophyll a and the early diversification of photosynthesis. PLoS One 11:e0151250
Clingenpeel S, Macur RE, Kan J, Inskeep WP, Lovalvo D, Varley J, Mathur E, Nealson K, Gorby Y, Jiang H, LaFracois T, McDermott TR (2011) Yellowstone lake: high-energy geochemistry and rich bacterial diversity. Environ Microbiol 13(8):2172–2185
DeBruyn JM, Nixon LT, Fawaz MN, Johnson AM, Radosevich M (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microbiol 77(17):6295–6300
DeBruyn JM, Fawaz MN, Peacock AD, Dunlap JR, Nixon LT, Cooper KE, Radosevich M (2013) Gemmatirosa kalamazoonesis gen. nov., sp nov., a member of the rarely-cultivated bacterial phylum Gemmatimonadetes. J Gen Appl Microbiol 59(4):305–312
Dueholm MS, Albertsen M, Stokholm-Bjerregaard M, McIlroy SJ, Karst SM, Nielsen PH (2015) Complete genome sequence of the bacterium Aalborg_AAW-1, representing a novel family within the candidate phylum SR1. Genome Announc 3(3)
Durbin AM, Teske A (2011) Microbial diversity and stratification of South Pacific abyssal marine sediments. Environ Microbiol 13:3219–3234
Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton Univ Press, Princeton, p 484
Fujita Y, Matsumoto H, Takahashi Y, Matsubara H (1993) Identification of a nifDK-like gene (ORF467) involved in the biosynthesis of chlorophyll in the cyanobacterium Plectonema boryanum. Plant Cell Physiol 34(2):305–314
Gest H, Blankenship RE (2004) Time line of discoveries: anoxygenic bacterial photosynthesis. Photosynth Res 80(1–3):59–70
Gest H, Favinger JL (1983) Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a “new” form of bacteriochlorophyll. Arch Microbiol 136(1):11–16
Gibson LCD, Willows RD, Kannangara CG, Von Wettstein D, Hunter CN (1995) Magnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: reconstitution of activity by combining the products of the bchH,-I, and-D genes expressed in Escherichia coli. Proc Natl Acad Sci U S A 92(6):1941–1944
Gugliandolo C, Michaud L, Lo Giudice A, Lentini V, Rochera C, Camacho A, Maugeri TL (2016) Prokaryotic community in lacustrine sediments of Byers Peninsula (Livingston Island, Maritime Antarctica). Microb Ecol 71:387–400
Hanada S, Sekiguchi Y (2014) The phylum Gemmatimonadetes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes - other major lineages of bacteria and the archaea. Springer, Berlin, pp 677–681
Haselkorn R, Lapidus A, Kogan Y, Vlcek C, Paces J, Paces V, Ulbrich P, Pecenkova T, Rebrekov D, Milgram A, Mazur M, Cox R, Kyrpides N, Ivanova N, Kapatral V, Los T, Lykidis A, Mikhailova N, Reznik G, Vasieva O, Fonstein M (2001) The Rhodobacter capsulatus genome. Photosynth Res 70(1):43–52
Hauruseu D, Koblizek M (2012) Influence of light on carbon utilization in aerobic anoxygenic phototrophs. Appl Environ Microbiol 78(20):7414–7419
Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548
Imhoff JF (2006) The phototrophic beta-proteobacteria. In: The prokaryotes. Springer, pp 593–601
Jung J, Choi S, Hong H, Sung J-S, Park W (2014) Effect of red clay on diesel bioremediation and soil bacterial community. Microb Ecol 68(2):314–323
Kamagata Y (2010) Phylum XXI. Gemmatimonadetes Zhang, Sekiguchi, Hanada, Hugenholtz, Kim, Kamagata and Nakamura 2003, 1161VP. In: Krieg NR, Staley JT, Brown DR et al. (eds) Bergey’s manual of systematic bacteriology, vol IV, 2 edn. Springer, New York, pp 781–784
Kamke J, Taylor MW, Schmitt S (2010) Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. ISME J 4:498–508
Kirchman DL, Hanson TE (2013) Bioenergetics of photoheterotrophic bacteria in the oceans. Environ Microbiol Rep 5(2):188–199
Koblížek M, Mlčoušková J, Kolber Z, Kopecký J (2010) On the photosynthetic properties of marine bacterium COL2P belonging to Roseobacter clade. Arch Microbiol 192(1):41–49
Lang AS, Beatty JT (2000) Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus. Proc Natl Acad Sci U S A 97(2):859–864
Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, Chisholm SW (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci U S A 101(30):11013–11018
Mann NH, Cook A, Millard A, Bailey S, Clokie M (2003) Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424(6950):741
Marrs B (1974) Genetic recombination in Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A 71(3):971–973
Marrs B (1981) Mobilization of the genes for photosynthesis from Rhodopseudomonas capsulata by a promiscuous plasmid. J Bacteriol 146(3):1003–1012
Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RAC (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinforma 9:386
Molisch H (1907) Die Purpurbakterien nach neuen Untersuchungen. Gustav Fischer, Jena, Germany
Nadson GA (1906) The morphology of inferior algae. III. Chlorobium limicola Nads., the green chlorophyll bearing microbe. Bull Jard Bot St Petersp 6:190
Nagashima S, Nagashima KV (2013) Comparison of photosynthesis gene clusters retrieved from total genome sequences of purple bacteria. In: Beatty JT (ed) Genome evolution of photosynthetic bacteria. Elsevier B.V., San Diego, pp 151–178
Nisbet EG, Sleep NH (2001) The habitat and nature of early life. Nature 409(6823):1083–1091
Olson JM (2006) Photosynthesis in the Archean Era. Photosynt Res 88:109–117
Overmann J, Garcia-Pichel F (2013) The phototrophic way of life. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic communities and ecophysiology, 4th edn. Springer, Berlin, pp 203–257
Pascual J, García-López M, Bills GF, Genilloud O (2016) Longimicrobium terrae gen. nov., sp. nov., a novel oligotrophic bacterium of the underrepresented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.000974
Petersen J, Brinkmann H, Bunk B, Michael V, Paeuker O, Pradella S (2012) Think pink: photosynthesis, plasmids and the Roseobacter clade. Environ Microbiol 14(10):2661–2672
Pierson BK, Castenholz Rw (1974) A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch Microbiol 100(1):5–24
Portillo MC, Leff JW, Lauber CL, Fierer N (2013) Cell size distributions of soil bacterial and archaeal taxa. Appl Environ Microbiol 79:7610–7617
Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58(4):755–805
Raymond J, Zhaxybayeva O, Gogarten JP, Gerdes SY, Blankenship RE (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298(5598):1616–1620
Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers Y-H, Falcon LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical pacific. PLoS Biol 5(3):398–431
Saunders AH, Golbeck JH, Bryant DA (2013) Characterization of BciB: a ferredoxin-dependent 8-vinyl-protochlorophyllide reductase from the green sulfur bacterium Chloroherpeton thalassium. Biochemistry 52(47):8442–8451
Schmidle W (1901) Neue Algen aus dem Gebiete des Oberrheins. Beih Bot Zentralbl 10:179–180
Selyanin V, Hauruseu D, Koblížek M (2016) The variability of light-harvesting complexes in aerobic anoxygenic phototrophs. Photosynth Res 128(1):35–43
Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F, Atamna-Ismaeel N, Pinter RY, Partensky F, Koonin EV, Wolf YI, Nelson N, Beja O (2009) Photosystem I gene cassettes are present in marine virus genomes. Nature 461(7261):258–262
Sheng P, Yu Y, Zhang G, Huang J, He L, Ding J (2016) Bacterial diversity and distribution in seven different estuarine sediments of Poyang Lake, China. Environ Earth Sci 75:479
Steffen MM, Li Z, Effler TC, Hauser LJ, Boyer GL, Wilhelm SW (2012) Comparative metagenomics of toxic freshwater cyanobacteria bloom communities on two continents. PLoS One 7(8)
Steven B, Gallegos-Graves LV, Yeager CM, Belnap J, Evans RD, Kuske CR (2012) Dryland biological soil crust cyanobacteria show unexpected decreases in abundance under long-term elevated CO2. Environ Microbiol 14(12):3247–3258
Swingley WD, Blankenship RE, Raymond J (2009) Evolutionary relationships among purple photosynthetic bacteria and the origin of proteobacterial photosynthetic systems. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) Advances in photosynthesis and respiration, the purple phototrophic bacteria, vol 28. Springer, Dordrecht, pp 17–29
Takaichi S, Maoka T, Takasaki K, Hanada S (2010) Carotenoids of Gemmatimonas aurantiaca (Gemmatimonadetes): identification of a novel carotenoid, deoxyoscillol 2-rhamnoside, and proposed biosynthetic pathway of oscillol 2, 2’-dirhamnoside. Microbiology 156(3):757–763
Tuorto SJ, Darias P, McGuinness LR, Panikov N, Zhang TJ, Haggblom MM, Kerkhof LJ (2014) Bacterial genome replication at subzero temperatures in permafrost. ISME J 8:139–149
Ulloa O, Canfield DE, DeLong EF, Letelier RM, Stewart FJ (2012) Microbial oceanography of anoxic oxygen minimum zones. Proc Natl Acad Sci U S A 109(40):15996–16003
Wang Z, Guo F, Liu L, Zhang T (2014) Evidence of carbon fixation pathway in a bacterium from candidate phylum SBR1093 revealed with genomic analysis. PLoS One 9(10), e109571
Winogradsky S (1888) Zur morphologie und Physiologie der Schwefelbakterien. Arthur Felix, Leipzig
Xiong J, Inoue K, Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci U S A 95(25):14851–14856
Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62(3):695–724
Zeng Y, Feng F, Medova H, Dean J, Koblizek M (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci U S A 111(21):7795–7800
Zeng Y, Selyanin V, Lukes M, Dean J, Kaftan D, Feng F, Koblížek M (2015) Characterization of the microaerophilic, bacteriochlorophyll a-containing bacterium Gemmatimonas phototrophica sp nov., and emended descriptions of the genus Gemmatimonas and Gemmatimonas aurantiaca. Int J Syst Evol Microbiol 65:2410–2419
Zeng Y, Baumbach J, Vieira Barbosa EG, Azevedo V, Zhang C, Koblížek M (2016) Metagenomic evidence for the presence of phototrophic Gemmatimonadetes bacteria in diverse environments. Environ Microbiol Rep 8(1):139–149
Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163
Zheng Q, Zhang R, Koblizek M, Boldareva EN, Yurkov V, Yan S, Jiao N (2011) Diverse arrangement of photosynthetic gene clusters in aerobic anoxygenic phototrophic bacteria. PLoS One 6(9):e25050
Zhou J, Sun D, Childers A, McDermott TR, Wang Y, Liles MR (2015) Three novel virophage genomes discovered from yellowstone lake metagenomes. J Virol 89(2):1278–1285
Acknowledgement
The main content of this chapter is a compilation of three research papers we published before (Zeng et al. 2014, 2015, 2016). We thank Fuying Feng, Hana Medová, Jason Dean, Vadim Selyanin, Martin Lukes, David Kaftan, and Jan Baumbach and his group members in University of Southern Denmark for their help in different periods along our journey of researching this novel phototrophic bacterial group. Y.Z.’s postdoctoral research in University of Southern Denmark was supported by the ERC advanced grant “OXYGEN.” M.K. would like to acknowledge the support from Czech projects GAČR P501/12/G055 and Algatech Plus LO1416.
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Zeng, Y., Koblížek, M. (2017). Phototrophic Gemmatimonadetes: A New “Purple” Branch on the Bacterial Tree of Life. In: Hallenbeck, P. (eds) Modern Topics in the Phototrophic Prokaryotes. Springer, Cham. https://doi.org/10.1007/978-3-319-46261-5_5
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