Rhizosphere heterogeneity shapes abundance and activity of sulfur-oxidizing bacteria in vegetated salt marsh sediments

Frontiers in Microbiology

Volumn 5, Issue JUN, 2014, Pages

  Thomas, François ^a,c   Giblin, Anne E ^b   Cardon, Zoe G ^b   Sievert, Stefan M ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b ECOSYSTEMS CENTER   (United States)

^c Faculté des Sciences et Technologies   (France)

Author keywords

RdsrAB; Rhizosphere; Salt marsh; SoxB; Spartina alterniflora; Sulfur oxidation

Indexed keywords

COMPLEMENTARY DNA; DNA 16S; TRANSCRIPTION FACTOR SOX;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GENE; BETAPROTEOBACTERIA; CELL HETEROGENEITY; CHEMOTAXONOMY; CHLOROBI; CHROMATIALES; DNA EXTRACTION; DNA SEQUENCE; DNA SYNTHESIS; EPSILONPROTEOBACTERIA; GENETIC TRANSCRIPTION; GRASS; MICROBIAL ACTIVITY; MICROBIAL BIOMASS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PLANT ROOT; RDSRAB GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHIZOSPHERE; RNA EXTRACTION; SALT MARSH; SEDIMENT; SPARTINA ALTERNIFLORA; SULFUR CYCLE; SULFUR OXIDIZING BACTERIUM; THIOTRICHALES; UNINDEXED SEQUENCE;

EID: 84904884966     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00309     Document Type: Article

References (67)

1. Akerman, N. H., Butterfield, D. A., and Huber, J. A. (2013). Phylogenetic diversity and functional gene patterns of sulfur-oxidizing subseafloor Epsilonproteobacteria in diffuse hydrothermal vent fluids. Front. Microbiol. 4:185. doi: 10.3389/fmicb.2013.00185
2. Bahr, M., Crump, B. C., Klepac-Ceraj, V., Teske, A., Sogin, M. L., and Hobbie, J. E. (2005). Molecular characterization of sulfate-reducing bacteria in a New England salt marsh. Environ. Microbiol. 7, 1175-1185. doi: 10.1111/j.1462-2920.2005.00796.x
3. Bradley, P. M., and Morris, J. T. (1990). Influence of oxygen and sulfide concentration on nitrogen uptake kinetics in Spartina alterniflora. Ecology 71, 282-287. doi: 10.2307/1940267
4. Bruckner, C. G., Mammitzsch, K., Jost, G., Wendt, J., Labrenz, M., and Jürgens, K. (2012). Chemolithoautotrophic denitrification of epsilonproteobacteria in marine pelagic redox gradients. Environ. Microbiol. 15, 1505-1513. doi: 10.1111/j.1462-2920.2012.02880.x
5. Brunet, R. C., and Garcia-Gil, L. J. (1996). Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments. FEMS Microbiol. Ecol. 21, 131-138. doi: 10.1111/j.1574-6941.1996.tb00340.x
6. Burgin, A. J., and Hamilton, S. K. (2007). Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front. Ecol. Environ. 5, 89-96. doi: 10.1890/1540-9295(2007)5[89:HWOTRO]2.0.CO;2
7. Campbell, B. J., Engel, A. S., Porter, M. L., and Takai, K. (2006). The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat. Rev. Microbiol. 4, 458-468. doi: 10.1038/nrmicro1414
8. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f.303
9. Davey, E., Wigand, C., Johnson, R., Sundberg, K., Morris, J., and Roman, C. T. (2011). Use of computed tomography imaging for quantifying coarse roots, rhizomes, peat, and particle densities in marsh soils. Ecol. Appl. 21, 2156-2171. doi: 10.1890/10-2037.1
10. Devereux, R., Hines, M., and Stahl, D. (1996). S Cycling: Characterization of natural communities of sulfate-reducing bacteria by 16S rRNA sequence comparisons. Microb. Ecol. 32, 283-292. doi: 10.1007/BF00183063
11. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
12. Eren, A. M., Vineis, J. H., Morrison, H. G., and Sogin, M. L. (2013). A filtering method to generate high quality short reads using Illumina paired-end technology. PLoS ONE 8:e66643. doi: 10.1371/journal.pone.0066643
13. Friedrich, C. G., Rother, D., Bardischewsky, F., Quentmeier, A., and Fischer, J. (2001). Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl. Environ. Microbiol. 67, 2873-2882. doi: 10.1128/AEM.67.7.2873-2882.2001
14. Fuchs, B. M., Spring, S., Teeling, H., Quast, C., Wulf, J., Schattenhofer, M., et al. (2007). Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 2891-2896. doi: 10.1073/pnas.0608046104
15. Ghosh, W., and Dam, B. (2009). Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol. Rev. 33, 999-1043. doi: 10.1111/j.1574-6976.2009.00187.x
16. Giblin, A. E., and Howarth, R. W. (1984). Porewater evidence for a dynamic sedimentary iron cycle in salt marshes. Limnol. Oceanogr. 29, 47-63. doi: 10.4319/lo.1984.29.1.0047
17. Giblin, A. E., and Wieder, R. K. (1992). "Sulphur cycling in marine and freshwater wetlands," in Sulphur Cycling on the Continents: Wetlands, Terrestrial Ecosystems, and Associated Water Bodies, eds R. W. Howarth, J. W. B. Steward, and M. V. Ivanov (Chichester: Jon Wiley and Sons), 85-117.
18. Grote, J., Jost, G., Labrenz, M., Herndl, G. J., and Jürgens, K. (2008). Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl. Environ. Microbiol. 74, 7546-7551. doi: 10.1128/AEM.01186-08
19. Hamersley, M. R., and Howes, B. L. (2005). Coupled nitrification-denitrification measured in situ in a Spartina alterniflora marsh with a 15NH+4 tracer. Mar. Ecol. Prog. Ser. 299, 123-135. doi: 10.3354/meps299123
20. Hines, M. E., Evans, R. S., Sharak Genthner, B. R., Willis, S. G., Friedman, S., Rooney-Varga, J. N., et al. (1999). Molecular phylogenetic and biogeochemical studies of sulfate-reducing bacteria in the rhizosphere of Spartina alterniflora. Appl. Environ. Microbiol. 65, 2209-2216.
21. Hines, M. E., Knollmeyer, S. L., and Tugel, J. B. (1989). Sulfate reduction and other sedimentary biogeochemistry in a northern New England salt marsh. Limnol. Oceanogr. 34, 578-590. doi: 10.4319/lo.1989.34.3.0578
22. Holmer, M., Gribsholt, B., and Kristensen, E. (2002). Effects of sea level rise on growth of Spartina anglica and oxygen dynamics in rhizosphere and salt marsh sediments. Mar. Ecol. Prog. Ser. 225, 197-204. doi: 10.3354/meps225197
23. Howarth, R. W., and Giblin, A. (1983). Sulfate reduction in the salt marshes at Sapelo Island, Georgia. Limnol. Oceanogr. 28, 70-82. doi: 10.4319/lo.1983.28.1.0070
24. Howarth, R. W., and Hobbie, J. E. (1982). "The regulation of decomposition and heterotrophic microbial activity in salt marsh soils: a review," in Estuarine Comparisons, ed V. S. Kennedy (New York, NY: Academic Press), 183-207.
25. Howarth, R. W., and Teal, J. M. (1980). Energy flow in a salt marsh ecosystem: the role of reduced inorganic sulfur compounds. Am. Nat. 116, 862-872. doi: 10.1086/283674
26. Huang, Y., Niu, B., Gao, Y., Fu, L., and Li, W. (2010). CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26, 680-682. doi: 10.1093/bioinformatics/btq003
27. Huber, J. A., Mark Welch, D. B., Morrison, H. G., Huse, S. M., Neal, P. R., Butterfield, D. A., et al. (2007). Microbial population structures in the deep marine biosphere. Science 318, 97-100. doi: 10.1126/science.1146689
28. Hügler, M., Gärtner, A., and Imhoff, J. F. (2010). Functional genes as markers for sulfur cycling and CO2 fixation in microbial communities of hydrothermal vents of the Logatchev field. FEMS Microbiol. Ecol. 73, 526-537. doi: 10.1111/j.1574-6941.2010.00919.x
29. Hügler, M., and Sievert, S. (2011). Beyond the calvin cycle: autotrophic carbon fixation in the ocean. Ann. Rev. Mar. Sci. 3, 261-289. doi: 10.1146/annurev-marine-120709-142712
30. Huse, S. M., Dethlefsen, L., Huber, J. A., Mark Welch, D., Welch, D. M., Relman, D. A., et al. (2008). Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. 4:e1000255. doi: 10.1371/journal.pgen.1000255
31. Joshi, M. M., and Hollis, J. P. (1977). Interaction of Beggiatoa and rice plant: detoxification of hydrogen sulfide in the rice rhizosphere. Science 195, 179-180. doi: 10.1126/science.195.4274.179
32. Kappler, U., and Dahl, C. (2001). Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol. Lett. 203, 1-9. doi: 10.1111/j.1574-6968.2001.tb10813.x
33. Katoh, K. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066. doi: 10.1093/nar/gkf436
34. Kelly, D. P., Shergill, J. K., Lu, W. P., and Wood, A. P. (1997). Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leeuwenhoek 71, 95-107. doi: 10.1023/A:1000135707181
35. King, G. M. (1988). Patterns of sulfate reduction and the sulfur cycle in a South Carolina salt marsh. Limnol. Oceanogr. 33, 376-390. doi: 10.4319/lo.1988.33.3.0376
36. Klepac-Ceraj, V., Bahr, M., Crump, B. C., Teske, A. P., Hobbie, J. E., and Polz, M. F. (2004). High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria. Environ. Microbiol. 6, 686-698. doi: 10.1111/j.1462-2920.2004.00600.x
37. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., et al. (2012). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 20, 1-11. doi: 10.1093/nar/gks808
38. Laverman, A. M., Pallud, C., Abell, J., and Van Cappellen, P. (2012). Comparative survey of potential nitrate and sulfate reduction rates in aquatic sediments. Geochim. Cosmochim. Acta 77, 474-488. doi: 10.1016/j.gca.2011.10.033
39. Lee, R. W. (1999). Oxidation of sulfide by Spartina alterniflora roots. Limnol. Oceanogr. 44, 1155-1159. doi: 10.4319/lo.1999.44.4.1155
40. Lenk, S., Arnds, J., Zerjatke, K., Musat, N., Amann, R., and Mussmann, M. (2011). Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment. Environ. Microbiol. 13, 758-774. doi: 10.1111/j.1462-2920.2010.02380.x
41. Lenk, S., Moraru, C., Hahnke, S., Arnds, J., Richter, M., Kube, M., et al. (2012). Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes. ISME J. 6, 2178-2187. doi: 10.1038/ismej.2012.66
42. Loy, A., Duller, S., Baranyi, C., Mussmann, M., Ott, J., Sharon, I., et al. (2009). Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes. Environ. Microbiol. 11, 289-299. doi: 10.1111/j.1462-2920.2008.01760.x
43. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., et al. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618. doi: 10.1038/ismej.2011.139
44. McMurdie, P. J., and Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of Microbiome census data. PLoS ONE 8:e61217. doi: 10.1371/journal.pone.0061217
45. Meyer, B., Imhoff, J. F., and Kuever, J. (2007). Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria - evolution of the Sox sulfur oxidation enzyme system. Environ. Microbiol. 9, 2957-2977. doi: 10.1111/j.1462-2920.2007.01407.x
46. Meyer, B., and Kuever, J. (2007). Molecular analysis of the diversity of sulfate-reducing and sulfur-oxidizing prokaryotes in the environment, using aprA as functional marker gene. Appl. Environ. Microbiol. 73, 7664-7679. doi: 10.1128/AEM.01272-07
47. Nelson, D. C., Waterbury, J. B., and Jannasch, H. W. (1982). Nitrogen fixation and nitrate utilization by marine and freshwater Beggiatoa. Arch. Microbiol. 133, 172-177. doi: 10.1007/BF00414997
48. Niemann, H., Linke, P., Knittel, K., Macpherson, E., Boetius, A., Brückmann, W., et al. (2013). Methane-carbon flow into the benthic food web at cold seeps - a case study from the Costa Rica subduction zone. PLoS ONE 8:e74894. doi: 10.1371/journal.pone.0074894
49. Niering, W. A., and Warren, R. S. (1980). Vegetation patterns and processes in New England salt marshes. Bioscience 30, 301-307. doi: 10.2307/1307853
50. Otte, S., Kuenen, J., Nielsen, L., Paerl, H., Zopfi, J., Schulz, H., et al. (1999). Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl. Environ. Microbiol. 65, 3148-3157.
51. Petri, R., Podgorsek, L., and Imhoff, J. F. (2001). Phylogeny and distribution of the soxB gene among thiosulfate-oxidizing bacteria. FEMS Microbiol. Lett. 197, 171-178. doi: 10.1111/j.1574-6968.2001.tb10600.x
52. Pezeshki, S. R., and Delaune, R. D. (1996). Responses of Spartina alterniflora and S. patens to rhizosphere oxygen deficiency. Acta Oecol. 17, 365-378.
53. Pott, A. S., and Dahl, C. (1998). Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144, 1881-1894. doi: 10.1099/00221287-144-7-1881
54. Robertson, L. A., and Kuenen, J. G. (2006). "The colorless sulfur bacteria," in The Prokaryotes, eds M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (New York, NY: Springer Verlag), 985-1011.
55. Ruby, E. G., and Jannasch, H. W. (1982). Physiological characteristics of Thiomicrospira sp. strain L-12 isolated from deep-sea hydrothermal vents. J. Bacteriol. 149, 161-165.
56. Sayama, M., Risgaard-Petersen, N., Nielsen, L. P., Fossing, H., and Christensen, P. B. (2005). Impact of bacterial NO-3 transport on sediment biogeochemistry. Appl. Environ. Microbiol. 71, 7575-7577. doi: 10.1128/AEM.71.11.7575-7577.2005
57. Schubauer, J. P., and Hopkinson, C. S. (1984). Above- and belowground emergent macrophyte production and turnover in a coastal marsh ecosystem, Georgia. Limnol. Oceanogr. 29, 1052-1065. doi: 10.4319/lo.1984.29.5.1052
58. Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., et al. (2011). Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60. doi: 10.1186/gb-2011-12-6-r60
59. Sievert, S. M., Kiene, R. P., and Shulz-Vogt, H. N. (2007). The sulfur cycle. Oceanography 41, 117-123. doi: 10.5670/oceanog.2007.55
60. Smith, C. J., Nedwell, D. B., Dong, L. F., and Osborn, A. M. (2006). Evaluation of quantitative polymerase chain reaction-based approaches for determining gene copy and gene transcript numbers in environmental samples. Environ. Microbiol. 8, 804-815. doi: 10.1111/j.1462-2920.2005.00963.x
61. Sorokin, D. Y., Tourova, T. P., Galinski, E. A., Muyzer, G., and Kuenen, J. G. (2008). Thiohalorhabdus denitrificans gen. nov., sp. nov., an extremely halophilic, sulfur-oxidizing, deep-lineage gammaproteobacterium from hypersaline habitats. Int. J. Syst. Evol. Microbiol. 58, 2890-2897. doi: 10.1099/ijs.0.2008/000166-0
62. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
63. Timmer-Ten Hoor, A. (1975). A new type of thiosulphate oxidizing, nitrate reducing microorganism: Thiomicrospira denitrificans sp. nov. Netherlands J. Sea Res. 9, 344-350. doi: 10.1016/0077-7579(75)90008-3
64. Tourova, T. P., Slobodova, N. V., Bumazhkin, B. K., Kolganova, T. V., Muyzer, G., and Sorokin, D. Y. (2013). Analysis of community composition of sulfur-oxidizing bacteria in hypersaline and soda lakes using soxB as a functional molecular marker. FEMS Microbiol. Ecol. 84, 280-289. doi: 10.1111/1574-6941.12056
65. Wirsen, C. O., and Jannasch, H. W. (1978). Physiological and morphological observations on Thiovulum sp. J. Bacteriol. 136, 765-774.
66. Wirsen, C. O., Sievert, S. M., Cavanaugh, C. M., Molyneaux, S. J., Ahmad, A., Taylor, L. T., et al. (2002). Characterization of an Autotrophic Sulfide-Oxidizing Marine Arcobacter sp. That Produces Filamentous Sulfur. Appl. Environ. Microbiol. 68, 316-325. doi: 10.1128/AEM.68.1.316-325.2002
67. Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., and Madden, T. L. (2012). Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. doi: 10.1186/1471-2105-13-134