Microbial Ecology

, Volume 73, Issue 3, pp 630–644 | Cite as

Microbial Community Functional Potential and Composition Are Shaped by Hydrologic Connectivity in Riverine Floodplain Soils

  • William A. Argiroff
  • Donald R. Zak
  • Christine M. Lanser
  • Michael J. Wiley
Soil Microbiology

Abstract

Riverine floodplains are ecologically and economically valuable ecosystems that are heavily threatened by anthropogenic stressors. Microbial communities in floodplain soils mediate critical biogeochemical processes, yet we understand little about the relationship between these communities and variation in hydrologic connectivity related to land management or topography. Here, we present metagenomic evidence that differences among microbial communities in three floodplain soils correspond to a long-term gradient of hydrologic connectivity. Specifically, all strictly anaerobic taxa and metabolic pathways were positively associated with increased hydrologic connectivity and flooding frequency. In contrast, most aerobic taxa and all strictly aerobic pathways were negatively related to hydrologic connectivity and flooding frequency. Furthermore, the genetic potential to metabolize organic compounds tended to decrease as hydrologic connectivity increased, which may reflect either the observed concomitant decline of soil organic matter or the parallel increase in both anaerobic taxa and pathways. A decline in soil N, accompanied by an increased genetic potential for oligotrophic N acquisition subsystems, suggests that soil nutrients also shape microbial communities in these soils. We conclude that differences among floodplain soil microbial communities can be conceptualized along a gradient of hydrologic connectivity. Additionally, we show that these differences are likely due to connectivity-related variation in flooding frequency, soil organic matter, and soil N. Our findings are particularly relevant to the restoration and management of microbially mediated biogeochemical processes in riverine floodplain wetlands.

Keywords

Microbial community Hydrologic connectivity Riverine floodplain Soil Wetland restoration 

Supplementary material

248_2016_883_MOESM1_ESM.pdf (704 kb)
ESM 1(PDF 704 kb)

References

  1. 1.
    Naiman RJ, Decamps H, Pollock M (1993) The role of riparian corridors in maintaining regional biodiversity. Ecol Appl 3:209–212. doi:10.2307/1941822 PubMedCrossRefGoogle Scholar
  2. 2.
    Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems. Can Spec Publ Fish Aquat Sci 106:110–127. doi:10.1371/journal.pone.0028909 Google Scholar
  3. 3.
    Tockner K, Stanford JA (2002) Riverine flood plains: present state and future trends. Environ Conserv 29:308–330. doi:10.1017/S037689290200022X CrossRefGoogle Scholar
  4. 4.
    Tockner K, Pennetzdorfer D, Reiner N et al (1999) Hydrological connectivity, and the exchange of organic matter and nutrients in a dynamic river-floodplain system (Danube, Austria). Freshw Biol 41:521–535. doi:10.1046/j.1365-2427.1999.00399.x CrossRefGoogle Scholar
  5. 5.
    Mitsch WJ, Day JW, Wendell Gilliam J et al (2001) Reducing nitrogen loading to the Gulf of Mexico from the Mississippi River Basin: strategies to counter a persistent ecological problem. Bioscience 51:373. doi:10.1641/0006-3568(2001)051[0373:RNLTTG]2.0.CO;2 CrossRefGoogle Scholar
  6. 6.
    Kousky C, Walls M (2014) Floodplain conservation as a flood mitigation strategy: examining costs and benefits. Ecol Econ 104:119–128. doi:10.1016/j.ecolecon.2014.05.001 CrossRefGoogle Scholar
  7. 7.
    Costanza R, Arge R, De Groot R et al (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260. doi:10.1038/387253a0 CrossRefGoogle Scholar
  8. 8.
    Tockner K, Pusch M, Borchardt D, Lorang MS (2010) Multiple stressors in coupled river-floodplain ecosystems. Freshw Biol 55:135–151. doi:10.1111/j.1365-2427.2009.02371.x CrossRefGoogle Scholar
  9. 9.
    Ward JV, Tockner K, Schiemer F (1999) Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regul Rivers Res Manag 15:125–139. doi:10.1002/(SICI)1099-1646(199901/06)15:1/3<125::AID-RRR523>3.0.CO;2-E CrossRefGoogle Scholar
  10. 10.
    Baker ME, Wiley MJ (2009) Multiscale control of flooding and riparian-forest composition in Lower Michigan, USA. Ecology 90:145–159. doi:10.1890/07-1242.1 PubMedCrossRefGoogle Scholar
  11. 11.
    Amoros C, Bornette G (2002) Connectivity and biocomplexity in waterbodies of riverine floodplains. Freshw Biol 47:761–776. doi:10.1046/j.1365-2427.2002.00905.x CrossRefGoogle Scholar
  12. 12.
    Kowalski KP, Wiley MJ, Wilcox D a (2014) Fish assemblages, connectivity, and habitat rehabilitation in a diked Great Lakes coastal wetland complex. Trans Am Fish Soc 143:1130–1142. doi:10.1080/00028487.2014.911207 CrossRefGoogle Scholar
  13. 13.
    Landress CM (2016) Fish assemblage associations with floodplain connectivity following restoration to benefit an endangered catostomid. Trans Am Fish Soc 145:83–93. doi:10.1080/00028487.2015.1105869 CrossRefGoogle Scholar
  14. 14.
    Morand A, Pierre J (1995) Habitat variability and space utilization by the amphibian communities of the French Upper-Rhone floodplain. Hydrobiologia 300–301:249–257. doi:10.1007/BF00024465 CrossRefGoogle Scholar
  15. 15.
    Van den Brink FWB, Van der Velde G, Wijnhoven S (2013) Seasonal changes in caddis larvae assemblages in river-floodplain habitats along a hydrological connectivity gradient. Hydrobiologia 716:75–85. doi:10.1007/s10750-013-1545-2 CrossRefGoogle Scholar
  16. 16.
    Van den Brink FWB, Van der Velde G, Buijse AD, Klink AG (1996) Biodiversity in the Lower Rhine and Meuse river-floodplains: its significance for ecological river management. Netherlands J Aquat Ecol 30:129–149. doi:10.1007/BF02272234 CrossRefGoogle Scholar
  17. 17.
    Keruzoré AA, Willby NJ, Gilvear DJ (2013) The role of lateral connectivity in the maintenance of macrophyte diversity and production in large rivers. Aquat Conserv Mar Freshw Ecosyst 23:301–315. doi:10.1002/aqc.2288 CrossRefGoogle Scholar
  18. 18.
    Moreno-Mateos D, Power ME, Comín FA, Yockteng R (2012) Structural and functional loss in restored wetland ecosystems. PLoS Biol 10:1–8. doi:10.1371/journal.pbio.1001247 CrossRefGoogle Scholar
  19. 19.
    Scott DT, Keim RF, Edwards BL et al (2014) Floodplain biogeochemical processing of floodwaters in the Atchafalaya River Basin during the Mississippi River flood of 2011. J Geophys Res Biogeosci 119:537–546. doi:10.1002/2013JG002477 CrossRefGoogle Scholar
  20. 20.
    Comin FA, Sánchez-Pérez JM, Español C et al (2016) Floodplain capacity to depollute water in relation to the structure of biological communities. Ecol Eng. doi:10.1016/j.ecoleng.2016.06.007 Google Scholar
  21. 21.
    Schlesinger WH, Bernhardt ES (2013) Biogeochemistry: an analysis of global change, 3rd edn. Academic/Elsevier, New YorkGoogle Scholar
  22. 22.
    Sha C, Mitsch WJ, Mander Ü et al (2011) Methane emissions from freshwater riverine wetlands. Ecol Eng 37:16–24. doi:10.1016/j.ecoleng.2010.07.022 CrossRefGoogle Scholar
  23. 23.
    Donner L, Ramanathan V (1980) Methane and nitrous oxide: their effects on the terrestrial climate. J Atmos Sci 37:119–124. doi:10.1175/1520-0469(1980)037<0119:MANOTE>2.0.CO;2 CrossRefGoogle Scholar
  24. 24.
    Kayranli B, Scholz M, Mustafa A, Hedmark Å (2010) Carbon storage and fluxes within freshwater wetlands: a critical review. Wetlands 30:111–124. doi:10.1007/s13157-009-0003-4 CrossRefGoogle Scholar
  25. 25.
    Fennessy MS, Mitsch WJ (2001) Effects of hydrology on spatial patterns of soil development in created riparian wetlands. Wetl Ecol Manag 9:103–120. doi:10.1023/A:1011104902410 CrossRefGoogle Scholar
  26. 26.
    Gallardo A (2003) Spatial variability of soil properties in a floodplain forest in northwest Spain. Ecosystems 6:564–576. doi:10.1007/s10021-003-0198-9 CrossRefGoogle Scholar
  27. 27.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631. doi:10.1073/pnas.0507535103 PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. doi:10.1890/05-1839 PubMedCrossRefGoogle Scholar
  29. 29.
    Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927. doi:10.1111/j.1365-2486.2012.02639.x CrossRefGoogle Scholar
  30. 30.
    Wagner D, Eisenhauer N, Cesarz S (2015) Plant species richness does not attenuate responses of soil microbial and nematode communities to a flood event. Soil Biol Biochem 89:135–149. doi:10.1016/j.soilbio.2015.07.001 CrossRefGoogle Scholar
  31. 31.
    Peralta AL, Matthews JW, Kent AD (2010) Microbial community structure and denitrification in a wetland mitigation bank. Appl Environ Microbiol 76:4207–4215. doi:10.1128/AEM.02977-09 PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Kemnitz D, Chin KJ, Bodelier P, Conrad R (2004) Community analysis of methanogenic archaea within a riparian flooding gradient. Environ Microbiol 6:449–461. doi:10.1111/j.1462-2920.2004.00573.x PubMedCrossRefGoogle Scholar
  33. 33.
    Rinklebe J, Langer U (2006) Microbial diversity in three floodplain soils at the Elbe River (Germany). Soil Biol Biochem 38:2144–2151. doi:10.1016/j.soilbio.2006.01.018 CrossRefGoogle Scholar
  34. 34.
    Ligi T, Truu M, Truu J et al (2014) Effects of soil chemical characteristics and water regime on denitrification genes (nirS, nirK, and nosZ) abundances in a created riverine wetland complex. Ecol Eng 72:47–55. doi:10.1016/j.ecoleng.2013.07.015 CrossRefGoogle Scholar
  35. 35.
    Moche M, Gutknecht J, Schulz E et al (2015) Monthly dynamics of microbial community structure and their controlling factors in three floodplain soils. Soil Biol Biochem 90:169–178. doi:10.1016/j.soilbio.2015.07.006 CrossRefGoogle Scholar
  36. 36.
    Tockner K, Malard F, Ward JV (2000) An extension of the flood pulse concept. Hydrol Process 14:2861–2883. doi:10.1002/1099-1085(200011/12)14:16/17<2861::AID-HYP124>3.0.CO;2-F CrossRefGoogle Scholar
  37. 37.
    Buchanan J, Chorbajian S, Dominguez A et al (2013) Restoring the Shiawassee Flats: estuarine gateway to Saginaw Bay. University of Michigan, Ann ArborGoogle Scholar
  38. 38.
    Frazier PS, Frazier PS, Page KJ, Page KJ (2000) Water body detection and delineation with Landsat TM data. Photogramm Eng Remote Sensing 66:1461–1467. doi:0099-1112I0OI6612-1461$3.00/0Google Scholar
  39. 39.
    Scott A (2014) Hydrology and nutrient flux in the Shiawassee Flats. University of Michigan, Ann ArborGoogle Scholar
  40. 40.
    Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  41. 41.
    Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. doi:10.14806/ej.17.1.200 CrossRefGoogle Scholar
  42. 42.
    Meyer F, Paarmann D, D’Souza M et al (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. doi:10.1186/1471-2105-9-386 PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Overbeek R, Begley T, Butler RM et al (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:5691–5702. doi:10.1093/nar/gki866 PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Overbeek R, Olson R, Pusch GD et al (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42:206–214. doi:10.1093/nar/gkt1226 CrossRefGoogle Scholar
  45. 45.
    Wilke A, Harrison T, Wilkening J et al (2012) The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinformatics. doi:10.1186/1471-2105-13-141 Google Scholar
  46. 46.
    Kirchman DL, Hanson TE, Cottrell MT, Hamdan LJ (2014) Metagenomic analysis of organic matter degradation in methane-rich Arctic Ocean sediments. Limnol Oceanogr 59:548–559. doi:10.4319/lo.2014.59.2.0548 CrossRefGoogle Scholar
  47. 47.
    R Core Team (2016) R: a language and environment for statistical computing. The R Foundation for Statistical Computing, ViennaGoogle Scholar
  48. 48.
    RStudio Team (2016) RStudio: integrated development for R. RStudio, BostonGoogle Scholar
  49. 49.
    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300Google Scholar
  50. 50.
    Franzosa EA, Morgan XC, Segata N et al (2014) Relating the metatranscriptome and metagenome of the human gut. Proc Natl Acad Sci U S A 111:E2329–E2338. doi:10.1073/pnas.1319284111 PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Li B, Yang Y, Ma L et al (2015) Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J 9:1–13. doi:10.1038/ismej.2015.59 CrossRefGoogle Scholar
  52. 52.
    Freedman ZB, Upchurch RA, Zak DR, Cline LC (2016) Anthropogenic N deposition slows decay by favoring bacterial metabolism: insights from metagenomic analyses. Front Microbiol 7:1–11. doi:10.3389/fmicb.2016.00259 CrossRefGoogle Scholar
  53. 53.
    Oksanen J, Blanchet FG, Kindt R, et al (2016) vegan: community ecology package. R package version 2.3-5. Available at https://CRAN.R-project.org/package=vegan
  54. 54.
    Anderson MJ (2001) A new method for non parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi:10.1111/j.1442-9993.2001.01070.pp.x Google Scholar
  55. 55.
    Clarke KR, Gorley RN (2006) PRIMER. PRIMER-E, PlymouthGoogle Scholar
  56. 56.
    Dworkin M, Falkow S, Rosenberg E, et al (2006) The Prokaryotes—volume 3: Archaea. Bacteria: Firmicutes, Actinomycetes, 3rd ed. doi:10.1007/0-387-30743-5Google Scholar
  57. 57.
    Jurado V, Gonzalez JM, Laiz L, Saiz-Jimenez C (2006) Aurantimonas altamirensis sp. nov., a member of the order Rhizobiales isolated from Altamira Cave. Int J Syst Evol Microbiol 56:2583–2585. doi:10.1099/ijs.0.64397-0 PubMedCrossRefGoogle Scholar
  58. 58.
    Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189. doi:10.1196/annals.1419.019 PubMedCrossRefGoogle Scholar
  59. 59.
    Schmidt TR, Scott EJ, Dyer DW (2011) Whole-genome phylogenies of the family Bacillaceae and expansion of the sigma factor gene family in the Bacillus cereus species-group. BMC Genomics 12:1–16. doi:10.1186/1471-2164-12-430 CrossRefGoogle Scholar
  60. 60.
    Rosenberg E, DeLong EF, Lory S et al (2014) The Prokaryotes—Deltaproteobacteria and Epsilonproteobacteria, 4th edn. Springer, Berlin. doi:10.1007/978-3-642-39044-9 Google Scholar
  61. 61.
    Rosenberg E, DeLong EF, Lory S et al (2014) The Prokaryotes—Gammaproteobacteria, 4th edn. Springer, Berlin. doi:10.1007/978-3-642-38922-1 CrossRefGoogle Scholar
  62. 62.
    Rosenberg E, DeLong EF, Lory S et al (2014) The Prokaryotes—other major lineages of Bacteria and the Archaea, 4th edn. Springer, Berlin. doi:10.1007/978-3-642-38954-2 Google Scholar
  63. 63.
    Rosenberg E, DeLong EF, Lory S et al (2014) The Prokaryotes—Actinobacteria, 4th edn. Springer, Berlin. doi:10.1007/978-3-642-30138-4 CrossRefGoogle Scholar
  64. 64.
    Rosenberg E, DeLong EF, Lory S et al (2014) The Prokaryotes—Firmicutes and Tenericutes, 4th edn. Springer, Berlin. doi:10.1007/978-3-642-30120-9 CrossRefGoogle Scholar
  65. 65.
    Rosenberg E, DeLong EF, Lory S et al (2014) The Prokaryotes—Alphaproteobacteria and Betaproteobacteria, 4th edn. Springer, Berlin. doi:10.1007/978-3-642-30197-1 CrossRefGoogle Scholar
  66. 66.
    Fonknechten N, Perret A, Perchat N et al (2009) A conserved gene cluster rules anaerobic oxidative degradation of L-ornithine. J Bacteriol 191:3162–3167. doi:10.1128/JB.01777-08 PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Porat I, Waters BW, Teng Q, Whitman WB (2004) Two biosynthetic pathways for aromatic amino acids in the archaeon Methanococcus maripaludis. J Bacteriol 186:4940–4950. doi:10.1128/JB.186.15.4940-4950.2004 PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Rastogi VK, Watson RJ (1991) Aspartate aminotransferase activity is required for aspartate catabolism and symbiotic nitrogen fixation in Rhizobium meliloti. J Bacteriol 173:2879–2887PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Dudley EG, Steele JL (2001) Lactococcus lactis LM0230 contains a single aminotransferase involved in aspartate biosynthesis, which is essential for growth in milk. Microbiology 147:215–224. doi:10.1099/00221287-147-1-215 PubMedCrossRefGoogle Scholar
  70. 70.
    Wyss M, Kaddurah-Daouk R (2000) Creatine and creatinine metabolism. Physiol Rev 80:1107–1213. doi:10.1016/S1286-0115(06)74505-2 PubMedGoogle Scholar
  71. 71.
    Harper CJ, Hayward D, Kidd M et al (2010) Glutamate dehydrogenase and glutamine synthetase are regulated in response to nitrogen availability in Myocbacterium smegmatis. BMC Microbiol 10:138. doi:10.1186/1471-2180-10-138 PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Ganesan B, Dobrowolski P, Weimer BC (2006) Identification of the leucine-to-2-methylbutyric acid catabolic pathway of Lactococcus lactis. Appl Environ Microbiol 72:4264–4273. doi:10.1128/AEM.00448-06 PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Mai X, Adams MWW (1994) Indolepyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus. A new enzyme involved in peptide fermentation. J Biol Chem 269:16726–16732PubMedGoogle Scholar
  74. 74.
    Sano K, Yokozeki K, Tamura F et al (1977) Microbial conversion of DL-2-amino-Δ 2-thiazoline-4-carboxylic acid to L-cysteine and L-cystine: screening of microorganisms and identification of products. Appl Environ Microbiol 34:806–810PubMedPubMedCentralGoogle Scholar
  75. 75.
    Velasco AM, Leguina JI, Lazcano A (2002) Molecular evolution of the lysine biosynthetic pathways. J Mol Evol 55:445–459. doi:10.1007/s00239-002-2340-2 PubMedCrossRefGoogle Scholar
  76. 76.
    Sekowska A, Dénervaud V, Ashida H et al (2004) Bacterial variations on the methionine salvage pathway. BMC Microbiol 4:9. doi:10.1186/1471-2180-4-9 PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Wendisch VF (1978) Amino acid biosynthesis. Annu Rev Biochem 47:533–606CrossRefGoogle Scholar
  78. 78.
    McGrath JW, Ternan NG, Quinn JP (1997) Utilization of organophosphonates by environmental micro-organisms. Lett Appl Microbiol 24:69–73. doi:10.1046/j.1472-765X.1997.00350.x CrossRefGoogle Scholar
  79. 79.
    Nemoto N, Kurihara S, Kitahara Y et al (2012) Mechanism for regulation of the putrescine utilization pathway by the transcription factor PuuR in Escherichia coli K-12. J Bacteriol 194:3437–3447. doi:10.1128/JB.00097-12 PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Mobley HLT, Hausinger RP (1989) Microbial ureases: significance, regulation, and molecular characterization. Microbiol Rev 53:85–108PubMedPubMedCentralGoogle Scholar
  81. 81.
    Claes WA, Puhler A, Kalinowski J (2002) Identification of two prpDBC gene clusters in Corynebacterium glutamicum and their involvement in propionate degradation via the 2-methylcitrate cycle. J Bacteriol 184:2728–2739. doi:10.1128/JB.184.10.2728-2739.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Freer SN (1993) Purification and characterization of the extracellular alpha-amylase from Streptococcus bovis JB1. Appl Environ Microbiol 59:1398–1402. doi: 0099-2240/93/051398-05$02.00/0Google Scholar
  83. 83.
    Tobisch S, Glaser P, Krüger S, Hecker M (1997) Identification and characterization of a new beta-glucoside utilization system in Bacillus subtilis. J Bacteriol 179:496–506PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Schwarz WH (2001) The cellulosome and cellulose degradation by anaerobic bacteria. Appl Microbiol Biotechnol 56:634–649. doi:10.1007/s002530100710 PubMedCrossRefGoogle Scholar
  85. 85.
    Yum D-Y, Lee B-Y, Pan J-G (1999) Identification of the yqhE and yafB genes encoding two 2, 5-diketo-D-gluconate reductases in Escherichia coli. Appl Environ Microbiol 65:3341–3346. doi:PMC91502Google Scholar
  86. 86.
    Shakeri-Garakani A, Brinkkötter A, Schmid K et al (2004) The genes and enzymes for the catabolism of galactitol, D-tagatose, and related carbohydrates in Klebsiella oxytoca M5a1 and other enteric bacteria display convergent evolution. Mol Genet Genomics 271:717–728. doi:10.1007/s00438-004-1022-8 PubMedCrossRefGoogle Scholar
  87. 87.
    Kato N, Yurimoto H, Thauer RK (2006) The physiological role of the ribulose monophosphate pathway in bacteria and archaea. Biosci Biotechnol Biochem 70:10–21. doi:10.1271/bbb.70.10 PubMedCrossRefGoogle Scholar
  88. 88.
    Arias A, Gardiol A, Martinez-Drets G (1982) Transport and catabolism of D-mannose in Rhizobium meliloti. J Bacteriol 151:1069–1072PubMedPubMedCentralGoogle Scholar
  89. 89.
    Munoz-Elias EJ, Upton AM, Cherian J, McKinney JD (2006) Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence. Mol Microbiol 60:1109–1122. doi:10.1111/j.1365-2958.2006.05155.x PubMedCrossRefGoogle Scholar
  90. 90.
    Cooper RA (1984) Metabolism of methylglyoxal in microorganisms. Annu Rev Microbiol 38:49–68. doi:10.1146/annurev.micro.38.1.49 PubMedCrossRefGoogle Scholar
  91. 91.
    McDonald IR, Bodrossy L, Chen Y, Murrell JC (2008) Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74:1305–1315. doi:10.1128/AEM.02233-07 PubMedCrossRefGoogle Scholar
  92. 92.
    Cusa E, Obradors N, Baldomà L et al (1999) Genetic analysis of a chromosomal region containing genes required for assimilation of allantoin nitrogen and linked glyoxylate metabolism in Escherichia coli genetic analysis of a chromosomal region containing genes required for assimilation of allantoin. J Bacteriol 181:7479–7484PubMedPubMedCentralGoogle Scholar
  93. 93.
    Kim SH, Oriel P (2000) Cloning and expression of the nitrile hydratase and amidase genes from Bacillus sp. BR449 into Escherichia coli. Enzyme Microb Technol 27:492–501. doi:10.1016/S0141-0229(00)00248-9 PubMedCrossRefGoogle Scholar
  94. 94.
    Ebbs S (2004) Biological degradation of cyanide compounds. Curr Opin Biotechnol 15:231–236. doi:10.1016/j.copbio.2004.03.006 PubMedCrossRefGoogle Scholar
  95. 95.
    Kobayashi M, Shimizu S (1994) Versatile nitrilases: nitrile-hydrolysing enzymes. FEMS Microbiol Lett 120:217–223. doi:10.1111/j.1574-6968.1994.tb07036.x CrossRefGoogle Scholar
  96. 96.
    Poole RK, Hughes MN (2000) New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol Microbiol 36:775–783. doi:10.1046/j.1365-2958.2000.01889.x PubMedCrossRefGoogle Scholar
  97. 97.
    Cook AM, Daughton CG, Alexander M (1978) Phosphonate utilization by bacteria. J Bacteriol 133:85–90PubMedPubMedCentralGoogle Scholar
  98. 98.
    Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:1–13. doi:10.3389/fmicb.2015.00402 CrossRefGoogle Scholar
  99. 99.
    McInerney MJ, Rohlin L, Mouttaki H et al (2007) The genome of Syntrophus aciditrophicus: life at the thermodynamic limit of microbial growth. Proc Natl Acad Sci U S A 104:7600–7605. doi:10.1073/pnas.0610456104 PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Michel H, Behr J, Harrenga A, Kannt A (1998) Cytochrome c oxidase: structure and spectroscopy. Annu Rev Biophys Biomol Struct 27:329–356. doi:10.1146/annurev.biophys.27.1.329 PubMedCrossRefGoogle Scholar
  101. 101.
    Pealing SL, Black AC, Manson FDC et al (1992) Sequence of the gene encoding flavocytochrome c from Shewanella putrefaciens: a tetraheme flavoenzyme that is a soluble fumarate reductase related to the membrane-bound enzymes. Biochemistry 31:12132–12140. doi:10.1021/bi00163a023 PubMedCrossRefGoogle Scholar
  102. 102.
    Galkin A, Kulakova L, Tishkov V et al (1995) Cloning of formate dehydrogenase gene from a methanol-utilizing bacterium Mycobacterium vaccae N10. Appl Microbiol Biotechnol 44:479–483. doi:10.1007/BF00169947 PubMedCrossRefGoogle Scholar
  103. 103.
    Kroger A, Geisler V, Lemma E et al (1992) Bacterial fumarate respiration. Arch Microbiol 158:311–314. doi:10.1007/BF00245358 CrossRefGoogle Scholar
  104. 104.
    Holliger C, Wohlfarth G, Diekert G (1999) Reductive dechlorination in the energy metabolism of anaerobic bacteria. FEMS Microbiol Rev 22:383–398. doi:10.1016/S0168-6445(98)00030-8 CrossRefGoogle Scholar
  105. 105.
    Dinamarca MA, Ruiz-Manzano A, Rojo F (2002) Inactivation of cytochrome o ubiquinol oxidase relieves catabolic repression of the Pseudomonas putida GPo1 alkane degradation pathway. J Bacteriol 184:3785–3793. doi:10.1128/JB.184.14.3785-3793.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Hensel M, Hinsley AP, Nikolaus T et al (1999) The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol Microbiol 32:275–287. doi:10.1046/j.1365-2958.1999.01345.x PubMedCrossRefGoogle Scholar
  107. 107.
    Barrett EL, Kwan HS (1985) Bacterial reduction of trimethylamine oxide. Annu Rev Microbiol 39:131–149PubMedCrossRefGoogle Scholar
  108. 108.
    Cook AM, Laue H, Junker F (1998) Microbial desulfonation. FEMS Microbiol Rev 22:399–419. doi:10.1016/S0168-6445(98)00028-X PubMedCrossRefGoogle Scholar
  109. 109.
    Miller TR, Belas R (2004) Dimethylsulfoniopropionate metabolism by Pfiesteria-associated Roseobacter spp. Appl Environ Microbiol 70:3383–3391. doi:10.1128/AEM.70.6.3383 PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    King JE, Quinn JP (1997) The utilization of organosulphonates by soil and freshwater bacteria. Lett Appl Microbiol 24:474–478. doi:10.1046/j.1472-765X.1997.00062.x CrossRefGoogle Scholar
  111. 111.
    Pophaly S, Singh R, Pophaly S et al (2012) Current status and emerging role of glutathione in food grade lactic acid bacteria. Microb Cell Fact 11:114. doi:10.1186/1475-2859-11-114 PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Bhandari V, Gupta RS (2014) The Phylum Thermotogae. In: Rosenberg E, DeLong EF, Lory S et al (eds) Prokaryotes—other major lineages Bact. Archaea, 4th edn. Springer, Berlin, pp 989–1015Google Scholar
  113. 113.
    Fierer N, Lauber CL, Ramirez KS et al (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. doi:10.1038/ismej.2011.159 PubMedCrossRefGoogle Scholar
  114. 114.
    Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160. doi:10.1111/j.1574-6941.2007.00375.x PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728. doi:10.1128/AEM.72.3.1719 PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14:300–306. doi:10.1016/j.mib.2011.04.007 PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    McNeil MM, Brown JM (1994) The medically important aerobic actinomycetes: epidemiology and microbiology. Clin Microbiol Rev 7:357–417. doi:10.1128/CMR.7.3.357 PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Ward NL, Challacombe JF, Janssen PH et al (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056. doi:10.1128/AEM.02294-08 PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Stackebrandt E (2014) The family Clostridiaceae, other genera. In: The Prokaryotes: Firmicutes and Tenericutes, 4th edn. Springer, Berlin, pp 67–73Google Scholar
  120. 120.
    Kuever J (2014) The family Desulfobacteraceae. In: The Prokaryotes: Deltaproteobacteria and Epsilonproteobacteria, 4th edn. Springer, Berlin, pp 45–73CrossRefGoogle Scholar
  121. 121.
    Kuever J, Galushko A (2014) The family Desulfomicrobiaceae. In: The Prokaryotes: Deltaproteobacteria and Epsilonproteobacteria, 4th edn. Springer, Berlin, pp 97–102CrossRefGoogle Scholar
  122. 122.
    Konhauser K (2009) Microbial metabolism. In: Introduction to geomicrobiology. Blackwell, Malden, pp 36–92Google Scholar
  123. 123.
    Canfield DE, Thamdrup B (2009) Towards a consistent classification scheme for geochemical environments, or, why we wish the term “suboxic” would go away: editorial. Geobiology 7:385–392. doi:10.1111/j.1472-4669.2009.00214.x PubMedCrossRefGoogle Scholar
  124. 124.
    Tiedje JM, Sexstone AJ, Parkin TB, Revsbech NP (1984) Anaerobic processes in soil. Plant Soil 76:197–212. doi:10.1007/BF02205580 CrossRefGoogle Scholar
  125. 125.
    Hernandez ME, Mitsch WJ (2007) Denitrification in created riverine wetlands: influence of hydrology and season. Ecol Eng 30:78–88. doi:10.1016/j.ecoleng.2007.01.015 CrossRefGoogle Scholar
  126. 126.
    Arah JRM (1997) Apportioning nitrous oxide fluxes between nitrification and denitrification using gas-phase mass spectrometry. Soil Biol Biochem 29:1295–1299. doi:10.1016/S0038-0717(97)00027-8 CrossRefGoogle Scholar
  127. 127.
    Peralta AL, Ludmer S, Kent AD (2013) Hydrologic history influences microbial community composition and nitrogen cycling under experimental drying/wetting treatments. Soil Biol Biochem 66:29–37. doi:10.1016/j.soilbio.2013.06.019 CrossRefGoogle Scholar
  128. 128.
    Peralta AL, Ludmer S, Matthews JW, Kent AD (2014) Bacterial community response to changes in soil redox potential along a moisture gradient in restored wetlands. Ecol Eng 73:246–253. doi:10.1016/j.ecoleng.2014.09.047 CrossRefGoogle Scholar
  129. 129.
    Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. doi:10.1128/AEM.00335-09 PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68. doi:10.1038/nature16069 PubMedCrossRefGoogle Scholar
  131. 131.
    Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843. doi:10.1016/S0038-0717(03)00123-8 CrossRefGoogle Scholar
  132. 132.
    Rillig MC, Caldwell BA, Wosten HAB, Sollins P (2007) Role of proteins in soil carbon and nitrogen storage: controls on persistence. Biogeochemistry 85:25–44. doi:10.1007/s10533-007-9102-6 CrossRefGoogle Scholar
  133. 133.
    Mitsch WJ, Bernal B, Nahlik AM et al (2013) Wetlands, carbon, and climate change. Landsc Ecol 28:583–597. doi:10.1007/s10980-012-9758-8 CrossRefGoogle Scholar
  134. 134.
    Six J, Paustian K, Elliott ET, Combrink C (2000) Soil structure and organic matter: I. Distribution of aggregate-size classes. Soil Sci Soc Am J 64:681–689. doi:10.2136/sssaj2000.642681x CrossRefGoogle Scholar
  135. 135.
    Maynard JJ, Dahlgren RA, O’Geen AT (2011) Soil carbon cycling and sequestration in a seasonally saturated wetland receiving agricultural runoff. Biogeosciences 8:3391–3406. doi:10.5194/bg-8-3391-2011 CrossRefGoogle Scholar
  136. 136.
    Prasse CE, Baldwin AH, Yarwood SA (2015) Site history and edaphic features override the influence of plant species on microbial communities in restored tidal freshwater wetlands. Appl Environ Microbiol 81:3482–3491. doi:10.1128/AEM.00038-15 PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631. doi:10.1038/nrmicro954 PubMedCrossRefGoogle Scholar
  138. 138.
    Zedler JB (2003) Wetlands at your service: reducing impacts of agriculture at the watershed scale. Front Ecol Environ 1:65–72. doi:10.1890/1540-9295(2003)001[0065:WAYSRI]2.0.CO;2 CrossRefGoogle Scholar
  139. 139.
    Zedler JB, Kercher S (2005) Wetland resources: status, trends, ecosystem services, and restorability. Annu Rev Environ Resour 30:39–74. doi:10.1146/annurev.energy.30.050504.144248 CrossRefGoogle Scholar
  140. 140.
    Mitsch WJ, Zhang L, Fink DF et al (2008) Ecological engineering of floodplains. Ecohydrol Hydrobiol 8:139–147. doi:10.2478/v10104-009-0010-3 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • William A. Argiroff
    • 1
  • Donald R. Zak
    • 1
    • 2
  • Christine M. Lanser
    • 1
  • Michael J. Wiley
    • 1
  1. 1.School of Natural Resources and EnvironmentUniversity of MichiganAnn ArborUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA

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