Lignocellulose-responsive bacteria in a southern california salt marsh identified by stable isotope probing

Frontiers in Microbiology

Volumn 5, Issue JUN, 2014, Pages 1-1

  Darjany, Lindsay E ^a   Whitcraft, Christine R ^a   Dillon, Jesse G ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Bacteria; Food web; Lignocellulose; Macrophytes; Salt marsh; Sediments; Stable isotope probing (SIP)

Indexed keywords

LIGNOCELLULOSE; STABLE ISOTOPE;

ARTICLE; BACTERIUM IDENTIFICATION; CARBON CYCLING; CARBON UTILIZATION; DNA EXTRACTION; FLAVOBACTERIA; GEL ELECTROPHORESIS; GENE AMPLIFICATION; GENE MUTATION; GENE SEQUENCE; GENETIC VARIABILITY; ISOTOPE ANALYSIS; MACROPHYTE; MASS SPECTROMETRY; MICROBIAL COMMUNITY; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SALT MARSH; SPECIES IDENTIFICATION; SPIROCHAETA; STABLE ISOTOPE PROBING; TERMINAL RESTRICTION FRAGMENT POLYMORPHISM;

EID: 84905198673     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00263     Document Type: Article

References (79)

1. Aneja, M. K., Sharma, S., Fleischmann, F., Stich, S., Heller, W., Bahnweg, G., et al. (2006). Microbial colonization of beech and spruce litter - Influence of decomposition site and plant litter species on the diversity of microbial community. Microb. Ecol. 52, 127-135. doi: 10.1007/s00248-006-9006-3
2. Ashelford, K. E., Chuzhanova, N. A., Fry, J. C., Jones, A. J., and Weightman, A. J. (2006). New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl. Environ. Microbiol. 72, 5734-5741. doi: 10.1128/AEM.00556-06
3. 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
4. Bastias, B. A., Anderson, I. C., Rangel-Castro, J. I., Parkin, P. I., Prosser, J. I., and Cairney, J. W. G. (2009). Influence of repeated prescribed burning on incorporation of 13C from cellulose by forest soil fungi as determined by RNA stable isotope probing. Soil Biol. Biochem. 41, 467-472. doi: 10.1016/j.soilbio.2008.11.018
5. Benner, R., Moran, M. A., and Hodson, R. E. (1986). Biogeochemical cycling of lignocellulosic carbon in marine and freshwater ecosystems relative contributions of prokaryotes and eukaryotes. Limnol. Oceanogr. 31, 89-100. doi: 10.4319/lo.1986.31.1.0089
6. Benner, R., Newell, S. Y., Maccubbin, A. E., and Hodson, R. E. (1984). Relative contributions of bacteria and fungi to rates of degradation of lignocellulosic detritus in salt-marsh sediments. Appl. Environ. Microbiol. 48, 36-40.
7. Berlanga, M., Paster, B. J., and Guerrero, R. (2010). Coevolution of symbiotic spirochete diversity in lower termites. Int. Microbiol. 10, 133-139.
8. Blum, L. K., Roberts, M. S., Garland, J. L., and Mills, A. L. (2004). Distribution of microbial communities associated with the dominant high marsh plants and sediments of the United States east coast. Microb. Ecol. 48, 375-388. doi: 10.1007/s00248-003-1051-6
9. Boschker, H. T. S., De Brouwer, J. F. C., and Cappenberg, T. E. (1999). The contribution of macrophyte-derived organic matter to microbial biomass in salt-marsh sediments: stable carbon isotope analysis of microbial biomarkers. Limnol. Oceanogr. 44, 309-319. doi: 10.4319/lo.1999.44.2.0309
10. Bouyoucos, G. J. (1962). Hydrometer method improved for making particle size analyses of soil. Agron. J. 54, 464-465. doi: 10.2134/agronj1962.00021962005400050028x
11. Breznak, J. A., and Warnecke, F. (2008). Spirochaeta cellobiosiphila sp. nov., a facultatively anaerobic, marine spirochaete. Int. J. Syst. Evol. Microbiol. 58, 2762-2768. doi: 10.1099/ijs.0.2008/001263-0
12. Buchan, A., Newell, S. Y., Butler, M., Biers, E. J., Hollibaugh, J. T., and Moran, M. A. (2003). Dynamics of bacterial and fungal communities on decaying salt marsh grass. Appl. Environ. Microbiol. 69, 6676-6687. doi: 10.1128/AEM.69.11.6676-6687.2003
13. Buckley, D. H., Huangyutitham, V., Hsu, S.-F., and Nelson, T. A. (2007). Stable isotope probing with 15N2 reveals novel noncultivated diazotrophs in soil. Appl. Environ. Microbiol. 73, 3196-3204. doi: 10.1128/AEM.02610-06
14. Buhring, S., Smittenberg, R., Sachse, D., Lipp, J., Golubic, S., Sachs, J., et al. (2009). A hypersaline microbial mat from the Pacific Atoll Kiritimati: insights into composition and carbon fixation using biomarker analyses and a 13C-labeling approach. Geobiology 7, 308-323. doi: 10.1111/j.1472-4669.2009.00198.x
15. Bushaw-Newton, K. L., Kreeger, D. A., Doaty, S., and Velinsky, D. J. (2008). Utilization of Spartina-and Phragmites-derived dissolved organic matter by bacteria and ribbed mussels (Geukensia demissa) from Delaware Bay salt marshes. Estuar. Coasts 31, 694-703. doi: 10.1007/s12237-008-9061-8
16. Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 265-270.
17. Chao, A., Lee, S. M., and Jeng, S. L. (1992). Estimating population size for capture-recapture data when capture probabilities vary by time and individual animal. Biometrics 201-216. doi: 10.2307/2532750
18. Chmura, G. L., Anisfeld, S. C., Cahoon, D. R., and Lynch, J. C. (2003). Global carbon sequestration in tidal, saline wetland soils. Global Biogeochem. Cycles 17. doi: 10.1029/2002GB001917
19. Choi, Y., Wang, Y., Hsieh, Y. Ä., and Robinson, L. (2001). Vegetation succession and carbon sequestration in a coastal wetland in northwest Florida: evidence from carbon isotopes. Global Biogeochem. Cycles 15, 311-319. doi: 10.1029/2000GB001308
20. Coffin, R. B., Velinsky, D. J., Devereux, R., Price, W. A., and Cifuentes, L. A. (1990). Stable carbon isotope analysis of nucleic acids to trace sources of dissolved substrates used by estuarine bacteria. Appl. Environ. Microbiol. 56, 2012-2020.
21. Das, M., Royer, T. V., and Leff, L. G. (2007). Diversity of fungi, bacteria, and actinomycetes on leaves decomposing in a stream. Appl. Environ. Microbiol. 73, 756-767. doi: 10.1128/AEM.01170-06
22. DeAngelis, K. M., Gladden, J. M., Allgaier, M., D'Haeseleer, P., Fortney, J. L., Reddy, A., et al. (2010). Strategies for enhancing the effectiveness of metagenomic-based enzyme discovery in lignocellulolytic microbial communities. Bioenerg. Res. 3, 146-158. doi: 10.1007/s12155-010-9089-z
23. Dillon, J. G., Mcmath, L. M., and Trout, A. L. (2009a). Seasonal changes in bacterial diversity in the Salton Sea. Hydrobiologia 632, 49-64. doi: 10.1007/s10750-009-9827-4
24. Dillon, J. G., Miller, S., Bebout, B., Hullar, M., Pinel, N., and Stahl, D. A. (2009b). Spatial and temporal variability in a stratified hypersaline microbial mat community. FEMS Microbiol. Ecol. 68, 46-58. doi: 10.1111/j.1574-6941.2009.00647.x
25. Droge, S., Rachel, R., Radek, R., and Konig, H. (2008). Treponema isoptericolens sp. nov., a novel spirochaete from the hindgut of the termite Incisitermes tabogae. Int. J. Syst. Evol. Microbiol. 58, 1079-1083. doi: 10.1099/ijs.0.64699-0
26. Eichorst, S. A., and Kuske, C. R. (2012). Identification of cellulose-responsive bacterial and fungal communities in geographically and edaphically different soils by using stable isotope probing. Appl. Environ. Microbiol. 78, 2316-2327. doi: 10.1128/AEM.07313-11
27. Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479-491.
28. Gallagher, J. L., Pfeiffer, W. J., and Pomeroy, L. R. (1976). Leaching and microbial utilization of dissolved organic carbon from leaves of Spartina alterniflora. Estuar. Coast. Mar. Sci. 4, 467-471. doi: 10.1016/0302-3524(76)90021-9
29. Good, I. J. (1953). The population frequencies of species and the estimation of population parameters. Biometrika 40, 237-264. doi: 10.1093/biomet/40.3-4.237
30. Haichar, F. E. Z., Achouak, W., Christen, R., Heulin, T., Marol, C., Marais, M.-F., et al. (2007). Identification of cellulolytic bacteria in soil by stable isotope probing. Environ. Microbiol. 9, 625-634. doi: 10.1111/j.1462-2920.2006.01182.x
31. Han, C., Sikorski, J., Lapidus, A., Nolan, M., Del Rio, T. G., Tice, H., et al. (2009). Complete genome sequence of Kangiella koreensis type strain (SW-125T). Stand. Genomic Sci. 1, 226. doi: 10.4056/sigs.36635
32. Harrison, B. K., and Orphan, V. J. (2012). Method for assessing mineral composition-dependent patterns in microbial diversity using magnetic and density separation. Geomicrobiol. J. 29, 435-449. doi: 10.1080/01490451.2011.581327
33. Hemminga, M., Kok, C., and De Munck, W. (1988). Decomposition of Spartina anglica roots and rhizomes in a salt marsh of the Westerschelde estuary. Mar. Ecol. Prog. Ser. 48.
34. 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
35. Hodson, R. E., Christian, R. R., and Maccubbin, A. E. (1984). Lignocellulose and lignin in the salt marsh grass Spartina alterniflora: initial concentrations and short-term, post-depositional changes in detrital matter. Mar. Biol. 81, 1-7. doi: 10.1007/BF00397619
36. Howarth, R. (1993). "Microbial processes in salt-marsh sediments," in Aquatic Microbiology, ed. T. E. Ford (Boston: Blackwell Scientific), 239-259.
37. Howarth, R. W., and Teal, J. M. (1979). Sulfate reduction in a New England USA salt marsh. Limnol. Oceanogr. 24, 999-1013. doi: 10.4319/lo.1979.24.6.0999
38. Hughes, J. B., and Hellmann, J. J. (2005). The application of rarefaction techniques to molecular inventories of microbial diversity. Methods Enzymol. 397, 292-308. doi: 10.1016/S0076-6879(05)97017-1
39. Hughes, J. B., Hellmann, J. J., Ricketts, T. H., and Bohannan, B. J. M. (2001). Counting the uncountable: statistical approaches to estimating microbial diversity. Appl. Environ. Microbiol. 67, 4399-4406. doi: 10.1128/AEM.67.10.4399-4406.2001
40. Hunter-Cevera, J. C. (1998). The value of microbial diversity. Curr. Opin. Microbiol. 1, 278-285. doi: 10.1016/S1369-5274(98)80030-1
41. Jean, W. D., Huang, S.-P., Chen, J.-S., and Shieh, W. Y. (2012). Kangiella taiwanensis sp. nov. and Kangiella marina sp. nov., marine bacteria isolated from shallow coastal water. Int. J. Syst. Evol. Microbiol. 62, 2229-2234. doi: 10.1099/ijs.0.037010-0
42. Keller, J. K., Takagi, K. K., Brown, M. E., Stump, K. N., Takahashi, C. G., Joo, W., et al. (2012). Soil organic carbon storage in restored salt marshes in Huntington Beach, California. Bull. South. Calif. Acad. Sci. 111, 153-161. doi: 10.3160/0038-3872-111.2.153
43. Khan, S. T., Nakagawa, Y., and Harayama, S. (2007). Sediminibacter furfurosus gen. nov., sp. nov. and Gilvibacter sediminis gen. nov., sp. nov., novel members of the family Flavobacteriaceae. Int. J. Syst. Evol. Microbiol. 57, 265-269. doi: 10.1099/ijs.0.64628-0
44. 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
45. Koretsky, C. M., Van Cappellen, P., Dichristina, T. J., Kostka, J. E., Lowe, K. L., Moore, C. M., et al. (2005). Salt marsh pore water geochemistry does not correlate with microbial community structure. Estuar. Coast. Shelf Sci. 62, 233-251. doi: 10.1016/j.ecss.2004.09.001
46. Kowalchuk, G., Buma, D., De Boer, W., Klinkhamer, P., and Van Veen, J. (2002). Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Anton. Leeuw. 81, 509-520. doi: 10.1023/A:1020565523615
47. Kwak, T. J., and Zedler, J. B. (1997). Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia (Berlin) 110, 262-277. doi: 10.1007/s004420050159
48. Liu, W., Marsh, T., Cheng, H., and Forney, L. (1997). Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63, 4516-4522.
49. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Kumar, Y., et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371. doi: 10.1093/nar/gkh293
50. Lydell, C., Dowell, L., Sikaroodi, M., Gillevet, P., and Emerson, D. (2004). A population survey of members of the phylum Bacteroidetes isolated from salt marsh sediments along the East Coast of the United States. Microb. Ecol. 48, 263-273. doi: 10.1007/s00248-003-1068-x
51. Margulis, L., Navarrete, A., and Sole, M. (2010). Cosmopolitan distribution of the large composite microbial mat spirochete, Spirosymplokos deltaeiberi. Int. Microbiol. 1, 27-34.
52. McCarthy, A. J. (1987). Lignocellulose-degrading actinomycetes. FEMS Microbiol. Lett. 46, 145-163. doi: 10.1111/j.1574-6968.1987.tb02456.x
53. Megonigal, J. P., Hines, M. E., and Visscher, P. T. (2004). "Anaerobic metabolism: linkages to trace gases and aerobic processes," in Biogeochemistry, ed. W. H. Schlesinger (Oxford: Elsevier-Pergamon), 317-434.
54. Minello, T. J., Able, K. W., Weinstein, M. P., and Hays, C. G. (2003). Salt marshes as nurseries for nekton: testing hypotheses on density, growth and survival through meta-analysis. Mar. Ecol. Prog. Ser. 246, 39-59. doi: 10.3354/meps246039
55. Mitsch, W. J., and Gosselink, J. G. (2007). Wetlands. Hoboken. New Jersey: Wiley.
56. Moran, M. A., and Hodson, R. E. (1990). Contributions of degrading Spartina alterniflora lignocellulose to the dissolved organic carbon pool of a salt marsh. Mar. Ecol. Prog. Ser. 62, 161-168. doi: 10.3354/meps062161
57. Mussmann, M., Ishii, K., Rabus, R., and Amann, R. (2005). Diversity and vertical distribution of cultured and uncultured Deltaproteobacteria in an intertidal mud flat of the Wadden Sea. Environ. Microbiol. 7, 405-418. doi: 10.1111/j.1462-2920.2005.00708.x
58. Muyzer, G., Teske, A., Wirsen, C. O., and Jannasch, H. W. (1995). Phylogenetic-relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel-electrophoresis of 16S rDNA fragments. Arch. Microbiol. 164, 165-172. doi: 10.1007/BF02529967
59. Neufeld, J. D., Vohra, J., Dumont, M. G., Lueders, T., Manefield, M., Friedrich, M. W., et al. (2007). DNA stable-isotope probing. Nat. Protoc. 2, 860-866. doi: 10.1038/nprot.2007.109
60. Neutel, A. M., Heesterbeek, J. A. P., and De Ruiter, P. C. (2002). Stability in real food webs: weak links in long loops. Science 296, 1120-1123. doi: 10.1126/science.1068326
61. Neutel, A. M., Heesterbeek, J. A. P., Van De Koppel, J., Hoenderboom, G., Vos, A., Kaldeway, C., et al. (2007). Reconciling complexity with stability in naturally assembling food webs. Nature 449, 599-602. doi: 10.1038/nature06154
62. Newell, S. Y. (1993). Decomposition of shoots of a salt-marsh grass: methodology and dynamics of microbial assemblages. Adv. Microb. Ecol. 13, 301-326. doi: 10.1007/978-1-4615-2858-6_7
63. Paerl, H. W., and Pinckney, J. L. (1996). A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microb. Ecol. 31, 225-247. doi: 10.1007/BF00171569
64. Peterson, B. J., Howarth, R. W., and Garritt, R. H. (1985). Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227, 1361-1363. doi: 10.1126/science.227.4692.1361
65. Prosser, J., Rangelcastro, J., and Killham, K. (2006). Studying plant-microbe interactions using stable isotope technologies. Curr. Opin. Biotechnol. 17, 98-102. doi: 10.1016/j.copbio.2006.01.001
66. Pruesse, E., Peplies, J., and Gloeckner, F. O. (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823-1829. doi: 10.1093/bioinformatics/bts252
67. Radajewski, S., Ineson, P., Parekh, N. R., and Murrell, J. C. (2000). Stable-isotope probing as a tool in microbial ecology. Nature 403, 646-649. doi: 10.1038/35001054
68. Romanenko, L. A., Tanaka, N., Frolova, G. M., and Mikhailov, V. V. (2010). Arenicella xantha gen. nov., sp. nov., a Gammaproteobacterium isolated from a marine sandy sediment. Int. J. Syst. Evol. Microbiol. 60, 1832-1836. doi: 10.1099/ijs.0.017194-0
69. Romani, A. M., Fischer, H., Mille-Lindblom, C., and Tranvik, L. J. (2006). Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. Ecology 87, 2559-2569. doi: 10.1890/0012-9658(2006)87[2559:IOBAFO]2.0.CO;2
70. Rooney-Varga, J. N., Genthner, B. R. S., Devereux, R., Willis, S. G., Friedman, S. D., and Hines, M. E. (1998). Phylogenetic and physiological diversity of sulphate-reducing bacteria isolated from a salt marsh sediment. Syst. Appl. Microbiol. 21, 557-568. doi: 10.1016/S0723-2020(98)80068-4
71. Schloss, P. D. (2008). Evaluating different approaches that test whether microbial communities have the same structure. ISME J. 2, 265-275. doi: 10.1038/ismej.2008.5
72. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541. doi: 10.1128/AEM.01541-09
73. Singleton, D. R., Furlong, M. A., Rathbun, S. L., and Whitman, W. B. (2001). Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl. Environ. Microbiol. 67, 4374-4376. doi: 10.1128/AEM.67.9.4374-4376.2001
74. So, C. M., and Young, L. Y. (1999). Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl. Environ. Microbiol. 65, 2969-2976.
75. Stackebrandt, E., and Goebel, B. M. (1994). Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44, 846-849. doi: 10.1099/00207713-44-4-846
76. Teal, T. H., Chapman, M., Guillemette, T., and Margulis, L. (1996). Free-living spirochetes from Cape Cod microbial mats detected by electron microscopy. Microbiologia 12, 571-584.
77. Wagner, K. I., Gallagher, S. K., Hayes, M., Lawrence, B. A., and Zedler, J. B. (2008). Wetland restoration in the new millennium: do research efforts match opportunities? Restor. Ecol. 16, 367-372. doi: 10.1111/j.1526-100X.2008.00433.x
78. Wilson, J. O. (1985). Decomposition of [14C] lignocelluloses of Spartina alterniflora and a comparison with field experiments. Appl. Environ. Microbiol. 49, 478-484.
79. Yoon, J. H., Oh, T. K., and Park, Y. H. (2004). Kangiella koreensis gen. nov., sp. nov. and Kangiella aquimarina sp. nov., isolated from a tidal flat of the Yellow Sea in Korea. Int. J. Syst. Evol. Microbiol. 54, 1829-1835. doi: 10.1099/ijs.0.63156-0