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Articles

Metabolic Responses of a Phototrophic Co-Culture Enriched from a Freshwater Sediment on Changing Substrate Availability and its Relevance for Biogeochemical Iron Cycling

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Pages 267-281 | Received 20 Apr 2020, Accepted 12 Oct 2020, Published online: 02 Nov 2020

References

  • Airs RL, Keely BJ. 2002. Atmospheric pressure chemical ionisation liquid chromatography/mass spectrometry of bacteriochlorophylls from Chlorobiaceae: characteristic fragmentations. Rapid Commun Mass Spectrom 16(5):453–461.
  • Baas-Becking LGM. 1934. Geobiologie of inleiding tot de milieukunde. The Hague, the Netherlands: W.P. van Stockum & Zoon.
  • Beatty JT, Overmann J, Lince MT, Manske AK, Lang AS, Blankenship RE, van Dover CL, Martinson TA, Plumley FG. 2005. An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci USA 102(26):9306–9310.
  • Begon M, Harper JL, Townsend CR. 1996. Ecology: Individuals, Populations and Communities. Oxford, UK: Blackwell Science Ltd.
  • Bóna-Lovász J. 2013. Metabolic analysis of carotenoid dynamics and global metabolism in carotenoid mutants of Rhodospirillum rubrum using HPLC/MS methodology [dissertation].  Stuttgart (BW): University of Stuttgart.
  • Bose A, Gardel EJ, Vidoudez C, Parra EA, Girguis PR. 2014. Electron uptake by iron-oxidizing phototrophic bacteria. Nat Commun 5:3391.
  • Brocks JJ, Love GD, Summons RE, Knoll AH, Logan GA, Bowden SA. 2005. Biomarker evidence for green and purple sulphur bacteria in a stratified palaeoproterozoic sea. Nature 437(7060):866–870.
  • Bryant DA, Liu Z, Li T, Zhao F, Costas AMG, Klatt CG, Ward DM, Frigaard NU, Overmann J. 2012. Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria. In: Burnap, RL and Vermaas, W, editors. Functional Genomics and Evolution of Photosynthetic Systems. Dordrecht: Springer, p47–102.
  • Bryce C, Franz-Wachtel M, Nalpas N, Miot J, Benzerara K, Byrne JM, Kleindienst S, Macek B, Kappler A. 2018a. Proteome response of a metabolically flexible anoxygenic phototroph to Fe(II) oxidation. Appl Environ Microbiol 84(16):e01166.
  • Bryce C, Blackwell N, Schmidt C, Otte J, Huang Y, Kleindienst S, Tomaszewski E, Schad M, Warter V, Peng C, et al. 2018b. Microbial anaerobic Fe(II) oxidation – ecology, mechanisms and environmental implications. Environ Microbiol 20(10):3462–3483.
  • Bryce C, Blackwell N, Straub D, Kleindienst S, Kappler A. 2019. Draft genome of Chlorobium sp. strain N1: a marine Fe(II)-oxidizing green sulfur bacterium. Microbiol Resour Announc 8(18):e00080.
  • Byrne JM, Klueglein N, Pearce C, Rosso KM, Appel E, Kappler A. 2015. Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria. Science 347(6229):1473–1476.
  • Canfield DE, Kristensen E, Thamdrup B. 2005. The sulfur cycle. Adv Mar Biol 48:313–381.
  • Caple MB, Chow HC, Strouse CE. 1978. Photosynthetic pigments of green sulfur bacteria. The esterifying alcohols of bacteriochlorophylls c from Chlorobium limicola. J Biol Chem 253(19):6730–6737.
  • Carbonero F, Oakley BB, Purdy KJ. 2014. Metabolic flexibility as a major predictor of spatial distribution in microbial communities. PLOS One 9(1):e85105.
  • Cook PLM, Wenzhöfer F, Glud RN, Janssen F, Huettel M. 2007. Benthic solute exchange and carbon mineralization in two shallow subtidal sandy sediments: Effect of advective pore‐water exchange. Limnol Oceanogr 52(5):1943–1963.
  • Crowe SA, Hahn AS, Morgan-Lang C, Thompson KJ, Simister RL, Lliros M, Hirst M, Hallam SJ. 2017. Draft genome sequence of the pelagic photoferrotroph Chlorobium phaeoferrooxidans. Genome Announc 5(13):e01584.
  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, et al. 2002. The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99(14):9509–9514.
  • Fixen KR, Zheng Y, Harris DF, Shaw S, Yang ZY, Dean DR, Seefeldt LC, Harwood CS. 2016. Light-driven carbon dioxide reduction to methane by nitrogenase in a photosynthetic bacterium. Proc Natl Acad Sci USA 113(36):10163–10167.
  • Garcia Costas AM, Tsukatani Y, Rijpstra WIC, Schouten S, Welander PV, Summons RE, Bryant DA. 2012. Identification of the bacteriochlorophylls, carotenoids, quinones, lipids, and hopanoids of “candidatus chloracidobacterium thermophilum". J Bacteriol 194(5):1158–1168.
  • Garrity GM, Holt JG, Overmann J, Pfennig N, Gibson J, Gorlenko VM. 2001. Phylum BXI. Chlorobi phy. nov.. In: Boone DR, Castenholz RW, Garrity GM, editors. Bergey’s Manual® of Systematic Bacteriology. New York (NY): Springer; p. 601–623.
  • Gasol JM, Jürgens K, Massana R, Calderón-Paz JI, Pedrós-Alió C. 1995. Mass development of Daphnia pulex in a sulphide-rich pond (Lake Cisó). Arch Hydrobiol 132:279–296.
  • Gilbert JA, Field D, Swift P, Newbold L, Oliver A, Smyth T, Somerfield PJ, Huse S, Joint I. 2009. The seasonal structure of microbial communities in the Western English Channel. Environ Microbiol 11(12):3132–3139.
  • Glaeser J, Overmann J. 2004. Biogeography, evolution, and diversity of epibionts in phototrophic consortia. Appl Environ Microbiol 70(8):4821–4830.
  • Gobet A, Böer SI, Huse SM, Van Beusekom JE, Quince C, Sogin ML, Boetius A, Ramette A. 2012. Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J 6(3):542–553.
  • Guerrero R, Berlanga M. 2006. Life’s unity and flexibility: the ecological link. Int Microbiol. 9:225–235.
  • Guzman MS, Rengasamy K, Binkley MM, Jones C, Ranaivoarisoa TO, Singh R, Fike DA, Meacham JM, Bose A. 2019. Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nat Commun. 10(1):1355.
  • Harwood CS, Gibson J. 1988. Anaerobic and aerobic metabolism of diverse aromatic compounds by the photosynthetic bacterium Rhodopseudomonas palustris. Appl Environ Microbiol 54(3):712–717.
  • Hegler F, Posth NR, Jiang J, Kappler A. 2008. Physiology of phototrophic iron(II)-oxidizing bacteria: implications for modern and ancient environments. FEMS Microbiol Ecol 66(2):250–260.
  • 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(2):116–124.
  • Huettel M, Webster IT. 2001. Porewater flow in permeable sediments. In: Bordeau, BP and Jorgensen BB, editors. The Benthic Boundary Layer: Transport Processes and Biogeochemistry. New York (NY): Oxford University Press, p. 144–179.
  • Imhoff JF. 2003. Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna-Matthews-Olson protein) gene sequences. Int J Syst Evol Microbiol 53(Pt 4):941–951.
  • Jiao Y, Kappler A, Croal L, Newman DK. 2005. Isolation and characterization of a genetically tractable photoautotrophic Fe(II)-oxidizing bacterium, Rhodopseudomonas palustris strain TIE-1. Appl Environ Microbiol 71(8):4487–4496.
  • Kappler A, Emerson D, Edwards K, Amend JP, Gralnick JA, Grathwohl P, Hoehler T, Straub KL. 2005. Microbial activity in biogeochemical gradients – new aspects of research. Geobiol 3(3):229–233.
  • Kassen R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evolution Biol 15(2):173–190.
  • Kim MK, Choi KM, Yin CR, Lee KY, Im WT, Lim JH, Lee ST. 2004. Odorous swine wastewater treatment by purple non-sulfur bacteria, Rhodopseudomonas palustris, isolated from eutrophicated ponds. Biotechnol Lett 26(10):819–822.
  • Kühl M, Lassen C, Jorgensen BB. 1994. Light penetration and light intensity in sandy marine sediments measured with irradiance and scalar irradiance fiber-optic microprobes. Mar Ecol Prog Ser 105:139–148.
  • Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Land ML, Pelletier DA, Beatty JT, Lang AS, et al. 2004. Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22(1):55–61.
  • Laufer K, Nordhoff M, Roy H, Schmidt C, Behrens S, Jorgensen BB, Kappler A. 2015. Coexistence of microaerophilic, nitrate-reducing, and phototrophic Fe(II) oxidizers and Fe(III) reducers in coastal marine sediment. Appl Environ Microbiol 82(5):1433–1447.
  • Laufer K, Niemeyer A, Nikeleit V, Halama M, Byrne JM, Kappler A. 2017. Physiological characterization of a halotolerant anoxygenic phototrophic Fe(II)-oxidizing green-sulfur bacterium isolated from a marine sediment. FEMS Microbiol Ecol 93(5):1–13.
  • Llirós M, García-Armisen T, Darchambeau F, Morana C, Triadó-Margarit X, Inceoğlu Ö, Borrego CM, Bouillon S, Servais P, Borges AV, et al. 2015. Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin. Sci Rep. 5:13803.
  • Lo KJ, Lin SS, Lu CW, Kuo CH, Liu CT. 2018. Whole-genome sequencing and comparative analysis of two plant-associated strains of Rhodopseudomonas palustris (PS3 and YSC3). Sci Rep 8(1):12769.
  • Lueder U, Jorgensen BB, Kappler A, Schmidt C. 2020. Fe(III) photoreduction as an important source of Fe(II) in oxic freshwater sediment. Environ Sci Technol 54(2):862–869.
  • 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(12):8049–8060.
  • Massé A, Pringault O, de Wit R. 2002. Experimental study of interactions between purple and green sulfur bacteria in sandy sediments exposed to illumination deprived of near-infrared wavelengths. Appl Environ Microbiol 68(6):2972–2981.
  • Mechsner K. 1957. Physiologische und morphologische Untersuchungen an Chlorobacterien. Archiv Mikrobiol 26(1):32–51.
  • Melton ED, Schmidt C, Behrens S, Schink B, Kappler A. 2014. Metabolic flexibility and substrate preference by the Fe (II)-oxidizing purple non-sulphur bacterium Rhodopseudomonas palustris strain Tie-1. Geomicrobiol J 31(9):835–843.
  • Morris BEL, Henneberger R, Huber H, Moissl-Eichinger C. 2013. Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37(3):384–406.
  • Muyzer G, De Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700.
  • Nadkarni MA, Martin FE, Jacques NA, Hunter N. 2002. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148(Pt 1):257–266.
  • Oda Y, Meijer WG, Gibson JL, Gottschal JC, Forney LJ. 2004. Analysis of diversity among 3-chlorobenzoate-degrading strains of rhodopseudomonas palustris. Microb. Ecol. 47(1):68–79. doi:10.1007/s00248-003-1028-5.
  • Oda Y, Larimer FW, Chain PSG, Malfatti S, Shin MV, Vergez LM, Hauser L, Land ML, Braatsch S, Beatty JT, et al. 2008. Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments. Proc Natl Acad Sci USA 105(47):18543–18548.
  • Otte J, Harter J, Laufer K, Blackwell N, Straub D, Kappler A, Kleindienst S. 2018. The distribution of active iron-cycling bacteria in marine and freshwater sediments is decoupled from geochemical gradients. Environ Microbiol 20(7):2483–2499.
  • Overmann J, Cypionka H, Pfennig N. 1992. An extremely low-light adapted phototrophic sulfur bacterium from the Black Sea. Limnol Oceanogr 37(1):150–155.
  • Overmann J, Schubert K. 2002. Phototrophic consortia: model systems for symbiotic interrelations between prokaryotes. Arch Microbiol 177(3):201–208.
  • Peng C, Bryce C, Sundman A, Kappler A. 2019. Cryptic cycling of Fe(III)-organic matter complexes by phototrophic Fe(II)-oxidizing bacteria. Appl Environ Microbiol 85(8):e02826.
  • Pfennig N. 1968. Chlorobium phaeobacteroides nov. spec. and C. phaeovibrioides nov. spec., two new species of green sulfur bacteria. Archiv Mikrobiol 63(3):224–226.
  • Pfennig N, Trüper HG. 1981. Isolation of members of the families Chromatiaceae and Chlorobiaceae. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG, editors. The Prokaryotes: A Handbook on Habitats, Isolation and Identification of Bacteria. Berlin: Springer.
  • Pierson BK, Sands VM, Frederick JL. 1990. Spectral irradiance and distribution of pigments in a highly layered marine microbial mat. Appl Environ Microbiol 56(8):2327–2340.
  • Plugge CM, Zhang WW, Scholten JCM, Stams AJ. 2011. Metabolic flexibility of sulfate-reducing bacteria. Front Microbiol 2:81.
  • Rivera SM, Christou P, Canela ‐ Garayoa R. 2014. Identification of carotenoids using mass spectrometry. Mass Spectrom Rev 33(5):353–372.
  • Sadekar S, Raymond J, Blankenship RE. 2006. Conservation of distantly related membrane proteins: photosynthetic reaction centers share a common structural core. Mol Biol Evol 23(11):2001–2007.
  • Schaedler F, Lockwood C, Lueder U, Glombitza C, Kappler A, Schmidt C. 2017. Microbially mediated coupling of Fe and n cycles by nitrate-reducing Fe(II)-oxidizing bacteria in littoral freshwater sediments. Appl Environ Microbiol 84(2):e0201317.
  • Schaedler S, Burkhardt C, Hegler F, Straub KL, Miot J, Benzerara K, Kappler A. 2009. Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria. Geomicrobiol J 26(2):93–103.
  • Schmidt C, Behrens S, Kappler A. 2010. Ecosystem functioning from a geomicrobiological perspective – a conceptual framework for biogeochemical iron cycling. Environ Chem 7(5):399–405.
  • Stomp M, Huisman J, Stal LJ, Matthijs HCP. 2007. Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule. Isme J 1(4):271–282.
  • Stookey LL. 1970. Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42(7):779–781.
  • Szafer W. 1911. Zur Kenntnis der Schwefelflora in der Umgebung von Lemberg. Bull Int Acad Sci Ser V Cracovie. :160–167.
  • Thompson KJ, Simister RL, Hahn AS, Hallam SJ, Crowe SA. 2017. Nutrient acquisition and the metabolic potential of photoferrotrophic chlorobi. Front Microbiol 8:1212.
  • Van Breemen RB, Dong L, Pajkovic ND. 2012. Atmospheric pressure chemical ionization tandem mass spectrometry of carotenoids. Int J Mass Spectrom 312:163–172.
  • Vila X, Abella CA. 1994. Effects of light quality on the physiology and the ecology of planktonic green sulfur bacteria in lakes. Photosynth Res 41(1):53–65.
  • Vogl K, Glaeser J, Pfannes KR, Wanner G, Overmann J. 2006. Chlorobium chlorochromatii sp. nov., a symbiotic green sulfur bacterium isolated from the phototrophic consortium ‘‘Chlorochromatium aggregatum. Arch Microbiol 185(5):363–372.
  • Walter XA, Picazo A, Miracle MR, Vicente E, Camacho A, Aragno M, Zopfi J. 2014. Phototrophic Fe(II)-oxidation in the chemocline of a ferruginous meromictic lake. Front Microbiol 5:713.
  • Whitman WB, Bowen TL, Boone DR. 2014. The methanogenic bacteria. p. 123–163. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E, editors, The Prokaryotes. New York, NY: Springer.
  • Widdel F, Pfennig N. 1981. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. I. Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov., sp. Nov. Arch Microbiol 129(5):395–400.
  • Widdel F. 1983. Methods for enrichment and pure culture isolation of filamentous gliding sulfate-reducing bacteria. Arch Microbiol 134(4):282–285.
  • Widdel F, Bak F. 1992. Gram-negative mesophilic sulfate-reducing bacteria. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH, editors. The Prokaryotes, 2nd ed., New York: Springer Verlag, p3352–3378.
  • Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B, Schink B. 1993. Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362(6423):834–836.
  • Wörmer L, Lipp JS, Schröder JM, Hinrichs KU. 2013. Application of two new LC–ESI–MS methods for improved detection of intact polar lipids (IPLs) in environmental samples. Org Geochem 59(59):10–21.
  • Wörmer L, Lipp J, Hinrichs KU. 2016. Comprehensive analysis of microbial lipids in environmental samples through HPLC-MS protocols. In: McGenity TJ, Timmis KN, Nogales B, editors, Hydrocarbon and lipid microbiology protocols. Berlin, Heidelberg: Springer Protocols Handbooks, p289–317.
  • Zarzycki J, Fuchs G. 2011. Coassimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl Environ Microbiol 77(17):6181–6188.

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