Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring

ISME Journal

Volumn 7, Issue 9, 2013, Pages 1775-1789

  Klatt, Christian G ^a,e   Liu, Zhenfeng ^b   Ludwig, Marcus ^b   Kühl, Michael ^c,d   Jensen, Sheila I ^c   Bryant, Donald A ^a,b   Ward, David M ^a,e  

^a MONTANA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^e SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

filamentous anoxygenic phototrophs; metagenomics; metatranscriptomics; mixotrophy; phototrophy

Indexed keywords

BACTERIOCHLOROPHYLL; CARBON; TRANSCRIPTOME;

CARBON DIOXIDE; CYANOBACTERIUM; ENVIRONMENTAL CONDITIONS; FERMENTATION; GENE EXPRESSION; METABOLISM; MICROBIAL COMMUNITY; MICROBIAL MAT; MIXOTROPHY; MUSHROOM; PHOTOAUTOTROPHY; RESOURCE AVAILABILITY; SPRING WATER;

ARTICLE; CHLOROFLEXI; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PHOTOPERIODICITY; PHOTOSYNTHESIS; THERMAL SPRING;

BACTERIOCHLOROPHYLLS; CARBON; CHLOROFLEXI; ENVIRONMENTAL MICROBIOLOGY; GENE EXPRESSION REGULATION, BACTERIAL; HOT SPRINGS; PHOTOPERIOD; PHOTOSYNTHESIS; TRANSCRIPTOME;

BASIDIOMYCOTA; CHLOROFLEXI; CHLOROFLEXI (CLASS); CHLOROFLEXUS; CYANOBACTERIA; ROSEIFLEXUS; SYNECHOCOCCUS;

EID: 84883152244     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.52     Document Type: Article

References (72)

1. Allewalt JP, Bateson MM, Revsbech NP, Slack K, Ward DM. (2006). Effect of temperature and light on growth of and photosynthesis by Synechococcus isolates typical of those predominating in the Octopus Spring microbial mat community of Yellowstone National Park. Appl Environ Microbiol 72: 544-550
2. Anderson KL, Tayne TA, Ward DM. (1987). Formation and fate of fermentation products in hot spring cyanobacterial mats. Appl Environ Microbiol 53: 2343-2352
3. Bassham JA, Kirk M. (1962). The effect of oxygen on the reduction of CO2 to glycolic acid and other products during photosynthesis by Chlorella. Biochem Biophys Res Commun 9: 376-380
4. Bateson MM, Ward DM. (1988). Photoexcretion and fate of glycolate in a hot spring cyanobacterial mat. Appl Environ Microbiol 54: 1738-1743
5. Bhaya D, Grossman AR, Steunou A-S, Khuri N, Cohan FM, Hamamura N et al. (2007). Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1: 703-713
6. Bryant DA, Costas AMG, Maresca JA, Chew AGM, Klatt CG, Bateson MM et al. (2007). Candidatus Chloracidobacterium thermophilum: An aerobic phototrophic Acidobacterium. Science 317: 523-526
7. Bryant DA, Klatt CG, Frigaard N-U, Liu Z, Li T, Zhao F et al. (2012). Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria. In: Burnap RL, Vermaas W (eds). Functional Genomics and Evolution of Photosynthetic Systems. Springer: Dordrecht, The Netherlands, pp 47-102
8. Buckel W, Golding BT. (2006). Radical enzymes in anaerobes. Ann Rev Microbiol 60: 27-49
9. Cao L, Bryant DA, Schepmoes AA, Vogl K, Smith RD, Lipton MS et al. (2012). Comparison of Chloroflexus aurantiacus strain J-10-fl proteomes of cells grown chemoheterotrophically and photoheterotrophically. Photosynth Res 110: 153-168
10. Doemel WN, Brock TD. (1977). Structure, growth, and decomposition of laminated algal-bacterial mats in alkaline hot springs. Appl Environ Microbiol 34: 433-452
11. Eisen MB, Spellman PT, Brown PO, Botstein D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868
12. Ferris MJ, Muyzer G, Ward DM. (1996). Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 62: 340-346
13. Gao X, Xin Y, Blankenship RE. (2009). Enzymatic activity of the alternative complex III as a menaquinol: Auracyanin oxidoreductase in the electron transfer chain of Chloroflexus aurantiacus. FEBS Lett 583: 3275-3279
14. Garcia Costas AM, Liu Z, Tomsho LP, Schuster SC, Ward DM, Bryant DA. (2012). Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria. Environ Microbiol 14: 177-190
15. Gregor J, Klug G. (1999). Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol Lett 179: 1-9
16. Hanada S, Pierson BK. (2006). The Family Chloroflexaceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds). The Prokaryotes Vol. 7. Springer: Berlin, pp 815-842
17. Hanada S, Takaichi S, Matsuura K, Nakamura K. (2002). Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes. Int J Syst Evol Microbiol 52: 187-193
18. Heda GD, Madigan MT. (1986). Utilization of amino acids and lack of diazotrophy in the thermophilic anoxygenic phototroph Chloroflexus aurantiacus. J Gen Microbiol 132: 2469-2473
19. Hesselmann RPX, von Rummell R, Resnick SM, Hany R, Zehnder AJB. (2000). Anaerobic metabolism of bacteria performing enhanced biological phosphate removal. Water Res 34: 3487-3494
20. Holo H, Sirevåg R. (1986). Autotrophic growth and CO2 fixation of Chloroflexus aurantiacus. Arch Microbiol 145: 173-180
21. Jensen SI, Steunou A-S, Bhaya D, Kühl M, Grossman AR. (2011). In situ dynamics of O2, pH and cyanobacterial transcripts associated with CCM, photosynthesis and detoxification of ROS. ISME J 5: 317-328
22. Keppen O, Baulina O, Kondratieva E. (1994). Oscillochloris trichoides neotype strain DG-6. Photosynth Res 41: 29-33
23. Keppen OI, Lebedeva NV, Troshina OY, Rodionov VY. (1989). The nitrogenase activity of a filamentous phototrophic green bacterium. Mikrobiologiya 58: 520-521
24. Klatt CG, Bryant DA, Ward DM. (2007). Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats. Environ Microbiol 9: 2067-2078
25. Klatt CG,Wood JM, Rusch DB, Bateson MM, Hamamura N, Heidelberg JF et al. (2011). Community ecology of hot spring cyanobacterial mats: Predominant populations and their functional potential. ISME J 5: 1262-1278
26. Knudsen E, Jantzen E, Bryn K, Ormerod JG, Sirevåg R. (1982). Quantitative and structural characteristics of lipids in Chlorobium and Chloroflexus. Arch Microbiol 132: 149-154
27. Kuznetsov BB, Ivanovsky RN, Keppen OI, Sukhacheva MV, Bumazhkin BK, Patutina EO et al. (2011). Draft genome sequence of the anoxygenic filamentous phototrophic bacterium Oscillochloris trichoides subsp. DG-6. J Bacteriol 193: 321-322
28. Lee M, del Rosario MC, Harris HH, Blankenship RE, Guss JM, Freeman HC. (2009). The crystal structure of auracyanin A at 1.85A ̊ resolution: The structures and functions of auracyanins A and B, two almost identical 'blue' copper proteins, in the photosynthetic bacterium Chloroflexus aurantiacus. J Biol Inorg Chem 14: 329-345
29. Li H, Durbin R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760
30. Liu Z, Klatt CG, Ludwig M, Rusch DB, Jensen SI, Kühl M et al. (2012). 'Candidatus Thermochlorobacter aerophilum': An aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics. ISME J 6: 1869-1882
31. Liu Z, Klatt CG, Wood JM, Rusch DB, Ludwig M, Wittekindt N et al. (2011). Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat. ISME J 5: 1279-1290
32. Ludwig M, Bryant DA. (2011). Transcription profiling of the model cyanobacterium Synechococcus sp. strain PCC 7002 by Next-Gen (SOLiDTM) sequencing of cDNA. Front Microbio 2: 41
33. Madigan MT, Petersen SR, Brock TD. (1974). Nutritional studies on Chloroflexus, a filamentous photosynthetic, gliding bacterium. Arch Microbiol 100: 97-103
34. McCool GJ, Cannon MC. (2001). PhaC and PhaR are required for polyhydroxyalkanoic acid synthase activity in Bacillus megaterium. J Bacteriol 183: 4235-4243
35. McManus JD, Brune DC, Han J, Sanders-Loehr J, Meyer TE, Cusanovich MA et al. (1992). Isolation, characterization, and amino acid sequences of auracyanins, blue copper proteins from the green photosynthetic bacterium Chloroflexus aurantiacus. J Biol Chem 267: 6531-6540
36. Nold SC, Ward DM. (1996). Photosynthate partitioning and fermentation in hot spring microbial mat communities. Appl Environ Microbiol 62: 4598-4607
37. Nübel U, Bateson MM, Vandieken V, Wieland A, Kuhl M, Ward DM. (2002). Microscopic examination of distribution and phenotypic properties of phylogenetically diverse Chloroflexaceae-related bacteria in hot spring microbial mats. Appl Environ Microbiol 68: 4593-4603
38. Oelze J. (1992). Light and oxygen regulation of the synthesis of bacteriochlorophylls a and c in Chloroflexus aurantiacus. J Bacteriol 174: 5021-5026
39. Ouchane S, Steunou A-S, Picaud M, Astier C. (2004). Aerobic and anaerobic Mg-protoporphyrin monomethyl ester cyclases in purple bacteria: A strategy adopted to bypass the repressive oxygen control system. J Biol Chem 279: 6385-6394
40. Pierson BK, Castenholz RW. (1974). A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch Microbiol 100: 5-24
41. Pinta V, Picaud M, Reiss-Husson F, Astier C. (2002). Rubrivivax gelatinosus acsF (previously Orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. J Bacteriol 184: 746-753
42. Ponnampalam SN, Buggy JJ, Bauer CE. (1995). Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light harvesting-II expression in Rhodobacter capsulatus. J Bacteriol 177: 2990-2997
43. Revsbech NP, Ward DM. (1984). Microelectrode studies of interstitial water chemistry and photosynthetic activity in a hot spring microbial mat. Appl Environ Microbiol 48: 270-275
44. Saldanha AJ. (2004). Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248
45. Sandbeck KA, Ward DM. (1981). Fate of immediate methane precursors in low-sulfate, hot-spring algal-bacterial mats. Appl Environ Microbiol 41: 775-782
46. Say RF, Fuchs G. (2010). Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 464: 1077-1081
47. Schaffert CS, Ward DM, Klatt CG, Pauley M, Steinke LA. (2012). Identification and distribution of high-Abundance proteins in the Octopus Spring microbial mat community. Appl Environ Microbiol 78: 8481-8484
48. Shiea J, Brassell SC, Ward DM. (1991). Comparative analysis of extractable lipids in hot spring microbial mats and their component photosynthetic bacteria. Org Geochem 17: 309-319
49. Steunou A-S, Bhaya D, Bateson MM, Melendrez MC, Ward DM, Brecht E et al. (2006). In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats. Proc Natl Acad Sci USA 103: 2398-2403
50. Steunou A-S, Jensen SI, Brecht E, Becraft ED, Bateson MM, Kilian O et al. (2008). Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat. ISME J 2: 364-378
51. Strauss G, Eisenreich W, Bacher A, Fuchs G. (1992). 13C-NMR study of autotrophic CO2 fixation pathways in the sulfur-reducing archaebacterium Thermoproteus neutrophilus and in the phototrphic eubacterium Chloroflexus aurantiacus. Eur J Biochem 214: 853-866
52. Strauss G, Fuchs G. (1993). Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle. Eur J Biochem 215: 633-643
53. Tang K-H, Barry K, Chertkov O, Dalin E, Han C, Hauser L et al. (2011). Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genomics 12: 334
54. Tang K-H, Wen J, Li X, Blankenship RE. (2009). Role of the AcsF protein in Chloroflexus aurantiacus. J Bacteriol 191: 3580-3587
55. Tourova TP, Spiridonova EM, Slobodova NV, Boulygina ES, Keppen OI, Kuznetsov BB et al. (2006). Phylogeny of anoxygenic filamentous phototrophic bacteria of the family Oscillochloridaceae as inferred from comparative analyses of the rrs, cbbL, and nifH genes. Mikrobiologiya 75: 192-200
56. Tsukatani Y, Nakayama N, Matsuura K, Shimada K, Hanada S, Nagashima K. (2007). Characterization of a blue copper protein auracyanin from the filamentous anoxygenic phototroph Roseiflexus castenholzii. Plant Cell Physiol 48: S73-S73
57. van der Meer MTJ, Klatt CG, Wood J, Bryant DA, Bateson MM, Lammerts L et al. (2010). Cultivation and genomic, nutritional, and lipid biomarker characterization of Roseiflexus strains closely related to predominant in situ populations inhabiting Yellowstone hot spring microbial mats. J Bacteriol 192: 3033-3042
58. van der Meer MTJ, Schouten S, Bateson MM, Nübel U, Wieland A, Kühl M et al. (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: 3978-3986
59. van der Meer MTJ, Schouten S, Sinninghe Damsté JS, de Leeuw JW, Ward DM. (2003). Compound-specific isotopic fractionation patterns suggest different carbon metabolisms among Chloroflexus-like bacteria in hotspring microbial mats. Appl Environ Microbiol 69: 6000-6006
60. van der Meer MTJ, Schouten S, Sinninghe Damsté JS, Ward DM. (2007). Impact of carbon metabolism on 13C signatures of cyanobacteria and green nonsulfur-like bacteria inhabiting a microbial mat from an alkaline siliceous hot spring in Yellowstone National Park (USA). Environ Microbiol 9: 482-491
61. van der Meer MTJ, Schouten S, van Dongen BE, Rijpstra WI, Fuchs G, Sinninghe Damsté JS et al. (2001). Biosynthetic controls on the 13C contents of organic components in the photoautotrophic bacterium Chloroflexus aurantiacus. J Biol Chem 276: 10971-10976
62. van Driessche G, Hu W, van de Werken G, Selvaraj F, McManus JD, Blankenship RE et al. (1999). Auracyanin A from the thermophilic green gliding photosynthetic bacterium Chloroflexus aurantiacus represents an unusual class of small blue copper proteins. Protein Sci 8: 947-957
63. Ward DM, Bateson MM, Ferris MJ, Kühl M, Wieland A, Koeppel A et al. (2006). Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, structure and function. Philos Trans R Soc Lond B Biol Sci 361: 1997-2008
64. Ward DM, Cohan FM, Bhaya D, Heidelberg JF, Kühl M, Grossman A. (2008). Genomics, environmental genomics and the issue ofmicrobial species. Heredity 100: 207-219
65. Ward DM, Weller R, Bateson MM. (1990). 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345: 63-65
66. Wu J, Bauer CE. (2008). RegB/RegA, a global redoxresponding two-component system. Adv Exp Med Biol 631: 131-148
67. Yanyushin MF, del Rosario MC, Brune DC, Blankenship RE. (2005). New class of bacterial membrane oxidoreductases. Biochemistry 44: 10037-10045
68. Yoon KS, Bobst C, Hemann CF, Hille R, Tabita FR. (2001). Spectroscopic and functional properties of novel 2[4Fe-4S] cluster-containing ferredoxins from the green sulfur bacterium Chlorobium tepidum. J Biol Chem 276: 44027-44036
69. Yoon KS, Hille R, Tabita FR. (1999). Rubredoxin from the green sulfur bacterium Chlorobium tepidum functions as an electron acceptor for pyruvate ferredoxin oxidoreductase. J Biol Chem 274: 29772-29778
70. Zappa S, Li K, Bauer CE. (2010). The tetrapyrrole biosynthetic pathway and its regulation in Rhodobacter capsulatus. Adv Exp Med Biol 675: 229-250
71. Zarzycki J, Brecht V, Müller M, Fuchs G. (2009). Identifying themissing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. Proc Natl Acad Sci USA 106: 21317-21322
72. Zarzycki J, Fuchs G. (2011). Co-Assimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl Environ Microbiol 77: 6181-6188