River Flow Impacts Bacterial and Archaeal Community Structure in Surface Sediments in the Northern Gulf of Mexico

  • Alice C. Ortmann
  • Pamela M. Brannock
  • Lei Wang
  • Kenneth M. Halanych
Environmental Microbiology

Abstract

Meiobenthic community structure in the northern Gulf of Mexico has been shown to be driven by geographical differences due to inshore–offshore gradients and location relative to river discharge. Samples collected along three transects spanning Mobile Bay, Alabama, showed significant differences in meiobenthic communities east of the bay compared to those sampled from the west. In contrast, analysis of bacterial and archaeal communities from the same sediment samples shows that the inshore–offshore gradient has minimal impact on their community structure. Significant differences in community structure were observed for Bacteria and Archaea between the east and west samples, but there was no difference in richness or diversity. Grouped by sediment type, higher richness was observed in silty samples compared to sandy samples. Significant differences were also observed among sediment types for community structure with bacteria communities in silty samples having more anaerobic sulfate reducers compared to aerobic heterotrophs, which had higher abundances in sandy sediments. This is likely due to increased organic matter in the silty sediments from the overlying river leading to low oxygen habitats. Most archaeal sequences represented poorly characterized high-level taxa, limiting interpretation of their distributions. Overlap between groups based on transect and sediment characteristics made determining which factor is more important in structuring bacterial and archaeal communities difficult. However, both factors are driven by discharge from the Mobile River. Although inshore–offshore gradients do not affect Bacteria or Archaea to the same extent as the meiobenthic communities, all three groups are strongly affected by sediment characteristics.

Keywords

Gulf of Mexico 16S rRNA Bacteria Archaea Sediment Community structure 

Notes

Acknowledgements

We thank Dr. Ron Kiene for the use of the multicorer as well as the crew members of the R/V E. O. Wilson. Thanks to Damien Waits for the help in sample collection and processing. This is Molette Biology Laboratory contribution #76 and Auburn University Marine Biology Program contribution #173.

Supplementary material

248_2018_1184_Fig5_ESM.gif (10 kb)
Fig. S1

Alpha diversity metrics for Archaea (A, B and C) and Bacteria (D, E and F) by transect. No significant differences were detected by ANOVA. (GIF 10 kb)

248_2018_1184_MOESM1_ESM.tif (3.6 mb)
High Resolution Image (TIFF 3652 kb)
248_2018_1184_Fig6_ESM.gif (10 kb)
Fig. S2

Alpha diversity metrics for Archaea (A, B and C) and Bacteria (D, E and F) by location. No significant differences were detected by ANOVA. (GIF 9 kb)

248_2018_1184_MOESM2_ESM.tif (3.6 mb)
High Resolution Image (TIFF 3652 kb)
248_2018_1184_MOESM3_ESM.docx (24 kb)
Table S1 (DOCX 24 kb)

References

  1. 1.
    O’Connor BS, Muller-Karger FE, Nero RW, Hu C, Peebles EB (2016) The role of Mississippi River discharge in offshore phytoplankton blooming in the northeastern Gulf of Mexico during August 2010. Remote Sens Environ 173:133–144CrossRefGoogle Scholar
  2. 2.
    Provoost P, Braeckman U, Van Gansbeke D, Moodley L, Soetaert K, Middelburg JJ, Vanaverbeke J (2013) Modelling benthic oxygen consumption and benthic-pelagic coupling at a shallow station in the southern North Sea. Estuar Coast Shelf Sci 120:1–11.  https://doi.org/10.1016/j.ecss.2013.01.008 CrossRefGoogle Scholar
  3. 3.
    Grippo MA, Fleeger JW, Rabalais NN, Condrey R, Carman KR (2010) Contribution of phytoplankton and benthic microalgae to inner shelf sediments of the north-central Gulf of Mexico. Cont Shelf Res 30:456–466.  https://doi.org/10.1016/j.csr.2009.12.015 CrossRefGoogle Scholar
  4. 4.
    Yazdani Foshtomi M, Braeckman U, Derycke S, Sapp M, Van Gansbeke D, Sabbe K, Willems A, Vincx M, Vanaverbeke J (2015) The link between microbial diversity and nitrogen cycling in marine sediments is modulated by macrofaunal bioturbation. PLoS One 10:e0130116.  https://doi.org/10.1371/journal.pone.0130116 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bernard RJ, Mortazavi B, Wang L, Ortmann AC, MacIntyre H, Burnett WC (2014) Benthic nutrient fluxes and limited denitrification in a sub-tropical groundwater-influenced coastal lagoon. Mar Ecol Prog Ser 504:13–26.  https://doi.org/10.3354/meps10783 CrossRefGoogle Scholar
  6. 6.
    Yang X, Huang S, Wu Q, Zhang R (2012) Nitrate reduction coupled with microbial oxidation of sulfide in river sediment. J Soils Sediments 12:1435–1444.  https://doi.org/10.1007/s11368-012-0542-9 CrossRefGoogle Scholar
  7. 7.
    Murrell MC, Fleeger JW (1989) Meiofauna abundance on the Gulf of Mexico continental shelf affected by hypoxia. Cont Shelf Res 9:1049–1062CrossRefGoogle Scholar
  8. 8.
    Levin LA, Ekau W, Gooday AJ, Jorissen F, Middelburg JJ, Naqvi SWA, Neira C, Rabalais NN, Zhang J (2009) Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6:2063–2098CrossRefGoogle Scholar
  9. 9.
    Schroeder WW, Wiseman Jr WJ (1999) Geology and hydrodynamics of Gulf of Mexico estuaries. In: Bianchi TS, Pennock JR, Twilley RR (eds) Biogeochemistry of Gulf of Mexico estuaries. Wiley, New York, pp 3–28Google Scholar
  10. 10.
    Kim C-K, Park K (2012) A modeling study of water and salt exchange for a micro-tidal, stratified northern Gulf of Mexico estuary. J Mar Syst 96–97:103–115.  https://doi.org/10.1016/j.jmarsys.2012.02.008 CrossRefGoogle Scholar
  11. 11.
    Bianchi TS, Pennock JR, Twilley RR (1999) Biogeochemistry of Gulf of Mexico estuaries: implications for management. In: Bianchi TS, Pennock JR, Twilley RR (eds) Biogeochemistry of Gulf of Mexico estuaries. Wiley, New York, pp 407–422Google Scholar
  12. 12.
    Wallace RK (1994) Mobile Bay and Alabama coastal waters fact sheet. Auburn University Marine Extension and Research Center, Sea Grant Extension, vol. ANR-919/MASGP 94-017Google Scholar
  13. 13.
    Brannock PM, Wang L, Ortmann AC, Waits DS, Halanych KM (2016) Genetic assessment of meiobenthic community composition and spatial distribution in coastal sediments along northern Gulf of Mexico. Mar Environ Res 119:166–175.  https://doi.org/10.1016/j.marenvres.2016.05.011 CrossRefPubMedGoogle Scholar
  14. 14.
    Newton RJ, Huse SM, Morrison HG, Peake CS, Sogin ML, McLellan SL (2013) Shifts in the microbial community composition of Gulf Coast beaches following beach oiling. PLoS One 8:e74265.  https://doi.org/10.1371/journal.pone.0074265 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Brady NC, Weil RR (1996) The nature and properties of soils, 11th ed. Prentice Hall, Inc., Upper Saddle RiverGoogle Scholar
  16. 16.
    Pennock JR, Cowan JLW (2001) Analytical instrumentation methods manual. In: Marine environmental sciences consortium technical report, vol 98-003. Dauphin Island Sea Lab, Dauphin IslandGoogle Scholar
  17. 17.
    Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Sparks DL, Page AL, Helmke PA, Loeppert RH (eds) Methods of soil analysis part 3, chemical methods. SSSA, ASA, Madison, pp 961–1010Google Scholar
  18. 18.
    Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Galand PE, Casamayor EO, Kirchman DL, Potvin M, Lovejoy C (2009) Unique archaeal assemblages in the Arctic Ocean unveiled by massively parallel tag sequencing. ISME J 3:860–869CrossRefPubMedGoogle Scholar
  21. 21.
    Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  23. 23.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of Bacteria and Archaea. ISME J 6:610–618.  https://doi.org/10.1038/ismej.2011.139 CrossRefPubMedGoogle Scholar
  25. 25.
    Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2009) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267.  https://doi.org/10.1093/bioinformatics/btp636 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59.  https://doi.org/10.1038/nmeth.2276 CrossRefPubMedGoogle Scholar
  27. 27.
    Brannock PM, Ortmann AC, Moss AG, Halanych KM (2016) Metabarcoding reveals environmental factors influencing spatio-temporal variation in pelagic micro-eukaryotes. Mol Ecol 25:3593–3604.  https://doi.org/10.1111/mec.13709 CrossRefPubMedGoogle Scholar
  28. 28.
    Ortmann AC, Ortell N (2014) Changes in free-living bacterial community diversity reflect the magnitude of environmental variability. FEMS Microbiol Ecol 87:291–301.  https://doi.org/10.1111/1574-6941.12225 CrossRefPubMedGoogle Scholar
  29. 29.
    R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, URL http://www.R-project.org/
  30. 30.
    Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693.  https://doi.org/10.1111/j.1461-0248.2006.00926.x CrossRefPubMedGoogle Scholar
  31. 31.
    Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R (2011) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protoc Bioinformatics Chapter 10:Unit 10.7.  https://doi.org/10.1002/0471250953.bi1007s36
  32. 32.
    Gaetano J (2013) Holm-Bonferroni sequential correction: an EXCEL calculator (1.2) [Microsoft Excel workbook]. https://www.researchgate.net/publication/242331583_Holm-Bonferroni_Sequential_Correction_An_EXCEL_Calculator_-_Ver._1.2. doi: https://doi.org/10.13140/RG.2.1.3920.0481
  33. 33.
    Fox J, Bouchet-Valat M (2016) Rcmdr: R commander. R package version 2.3–1Google Scholar
  34. 34.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124.  https://doi.org/10.1093/bioinformatics/btu494 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196.  https://doi.org/10.1093/nar/gkm864 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596.  https://doi.org/10.1093/nar/gks1219 CrossRefPubMedGoogle Scholar
  38. 38.
    Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glockner FO (2014) The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res 42:D643–D648.  https://doi.org/10.1093/nar/gkt1209 CrossRefPubMedGoogle Scholar
  39. 39.
    Spang A, Saw JH, Jorgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, van Eijk R, Schleper C, Guy L, Ettema TJG (2015) Complex Archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179.  https://doi.org/10.1038/nature14447 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Meng J, Xu J, Qin D, He Y, Xiao X, Wang F (2014) Genetic and functional properties of uncultivated MCG Archaea assessed by metagenome and gene expression analyses. ISME J 8:650–659.  https://doi.org/10.1038/ismej.2013.174 CrossRefPubMedGoogle Scholar
  41. 41.
    Mills HJ, Hunter E, Humphrys M, Kerkhof L, McGuinness L, Huettel M, Kostka JE (2008) Characterization of nitrifying, denitrifying, and overall bacterial communities in permeable marine sediments of the northeastern Gulf of Mexico. Appl Environ Microbiol 74:4440–4453.  https://doi.org/10.1128/aem.02692-07 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Lallias D, Hiddink JG, Fonseca VG, Gaspar JM, Sung W, Neill SP, Barnes N, Ferrero T, Hall N, Lambshead PJ, Packer M, Thomas WK, Creer S (2015) Environmental metabarcoding reveals heterogeneous drivers of microbial eukaryote diversity in contrasting estuarine ecosystems. ISME J 9:1208–1221.  https://doi.org/10.1038/ismej.2014.213 CrossRefPubMedGoogle Scholar
  43. 43.
    Feng BW, Li XR, Wang JH, Hu ZY, Meng H, Xiang LY, Quan ZX (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiol Ecol 70:80–92.  https://doi.org/10.1111/j.1574-6941.2009.00772.x CrossRefPubMedGoogle Scholar
  44. 44.
    Webster G, O’Sullivan LA, Meng Y, Williams AS, Sass AM, Watkins AJ, Parkes RJ, Weightman AJ (2015) Archaeal community diversity and abundance changes along a natural salinity gradient in estuarine sediments. FEMS Microbiol Ecol 91:1–18.  https://doi.org/10.1093/femsec/fiu025 CrossRefPubMedGoogle Scholar
  45. 45.
    Park K, Kim CK, Schroeder WW (2007) Temporal variability in summertime bottom hypoxia in shallow areas of Mobile Bay, Alabama. Estuar Coast 30:54–65CrossRefGoogle Scholar
  46. 46.
    Lazar CS, Biddle JF, Meador TB, Blair N, Hinrichs KU, Teske AP (2015) Environmental controls on intragroup diversity of the uncultured benthic Archaea of the Miscellaneous Crenarchaeotal group lineage naturally enriched in anoxic sediments of the White Oak River estuary (North Carolina, USA). Environ Microbiol 17:2228–2238.  https://doi.org/10.1111/1462-2920.12659 CrossRefPubMedGoogle Scholar
  47. 47.
    Devereux R, Mosher JJ, Vishnivetskaya TA, Brown SD, Beddick Jr DL, Yates DF, Palumbo AV (2015) Changes in northern Gulf of Mexico sediment bacterial and archaeal communities exposed to hypoxia. Geobiology 13:478–493.  https://doi.org/10.1111/gbi.12142 CrossRefPubMedGoogle Scholar
  48. 48.
    Rusch A, Hannides A, Gaidos E (2009) Diverse communities of active Bacteria and Archaea along oxygen gradients in coral reef sediments. Coral Reefs 28:15–26CrossRefGoogle Scholar
  49. 49.
    Imhoff JF, Hiraishi A, Suling J (2005) Anoxygenic phototrophic purple bacteria. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual® of systematic bacteriology. Springer, New York, pp 119–132CrossRefGoogle Scholar
  50. 50.
    Cleary DFR, Coelho FJRC, Oliveira V, Gomes NCM, Polónia ARM (2017) Sediment depth and habitat as predictors of the diversity and composition of sediment bacterial communities in an inter-tidal estuarine environment. Mar Ecol.  https://doi.org/10.1111/maec.12411
  51. 51.
    Gobet A, Boer 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 6:542–553.  https://doi.org/10.1038/ismej.2011.132 CrossRefPubMedGoogle Scholar
  52. 52.
    Xiong J, Ye X, Wang K, Chen H, Hu C, Zhu J, Zhang D (2014) Biogeography of the sediment bacterial community responds to a nitrogen pollution gradient in the East China Sea. Appl Environ Microbiol 80:1919–1925.  https://doi.org/10.1128/AEM.03731-13 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Teske A, Sorensen KB (2008) Uncultured Archaea in deep marine subsurface sediments: have we caught them all? ISME J 2:3–18CrossRefPubMedGoogle Scholar
  54. 54.
    Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356:148–149CrossRefPubMedGoogle Scholar
  55. 55.
    Webster G, Sass H, Cragg BA, Gorra R, Knab NJ, Green CJ, Mathes F, Fry JC, Weightman AJ, Parkes RJ (2011) Enrichment and cultivation of prokaryotes associated with the sulphate-methane transition zone of diffusion-controlled sediments of Aarhus Bay, Denmark, under heterotrophic conditions. FEMS Microbiol Ecol 77:248–263.  https://doi.org/10.1111/j.1574-6941.2011.01109.x CrossRefPubMedGoogle Scholar
  56. 56.
    Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stepanauskas R, Richter M, Kleindienst S, Lenk S (2013) Predominant Archaea in marine sediments degrade detrital proteins. Nature 496:215–218CrossRefPubMedGoogle Scholar
  57. 57.
    O’Sullivan LA, Sass AM, Webster G, Fry JC, Parkes RJ, Weightman AJ (2013) Contrasting relationships between biogeochemistry and prokaryotic diversity depth profiles along an estuarine sediment gradient. FEMS Microbiol Ecol 85:143–157.  https://doi.org/10.1111/1574-6941.12106 CrossRefPubMedGoogle Scholar
  58. 58.
    Na H, Lever MA, Kjeldsen KU, Schulz F, Jorgensen BB (2015) Uncultured Desulfobacteraceae and Crenarchaeotal group C3 incorporate 13C-acetate in coastal marine sediment. Environ Microbiol Rep 7:614–622.  https://doi.org/10.1111/1758-2229.12296 CrossRefPubMedGoogle Scholar
  59. 59.
    Pfeffer C, Larsen S, Song J, Dong M, Besenbacher F, Meyer RL, Kjeldsen KU, Schreiber L, Gorby YA, El-Naggar MY, Leung KM, Schramm A, Risgaard-Petersen N, Nielsen LP (2012) Filamentous bacteria transport electrons over centimetre distances. Nature 491:218–221.  https://doi.org/10.1038/nature11586 CrossRefPubMedGoogle Scholar
  60. 60.
    Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546CrossRefPubMedGoogle Scholar
  61. 61.
    Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damste JS, Rhee SK (2010) Cultivation of autotrophic ammonia-oxidizing Archaea from marine sediments in coculture with sulfur-oxidizing Bacteria. Appl Environ Microbiol 76:7575–7587.  https://doi.org/10.1128/AEM.01478-10 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Kubo K, Lloyd KG, FB J, Amann R, Teske A, Knittel K (2012) Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME J 6:1949–1965.  https://doi.org/10.1038/ismej.2012.37 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Fillol M, Auguet JC, Casamayor EO, Borrego CM (2016) Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage. ISME J 10:665–677.  https://doi.org/10.1038/ismej.2015.143 CrossRefPubMedGoogle Scholar
  64. 64.
    Lazar CS, Baker BJ, Seitz K, Hyde AS, Dick GJ, Hinrichs KU, Teske AP (2016) Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol 18:1200–1211.  https://doi.org/10.1111/1462-2920.13142 CrossRefPubMedGoogle Scholar
  65. 65.
    Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB, Anderson R, Fredricks HF, Elvert M, Kelly TJ, Schrag DP, Sogin ML, Brenchley JE, Teske A, House CH, Hinrichs K-U (2006) Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA 103:3846–3851.  https://doi.org/10.1073/pnas.0600035103 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Sun MY, Dafforn KA, Johnston EL, Brown MV (2013) Core sediment bacteria drive community response to anthropogenic contamination over multiple environmental gradients. Environ Microbiol 15:2517–2531.  https://doi.org/10.1111/1462-2920.12133 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Marine SciencesUniversity of South AlabamaMobileUSA
  2. 2.Dauphin Island Sea LabDauphin IslandUSA
  3. 3.Bedford Institute of OceanographyFisheries and Oceans CanadaDartmouthCanada
  4. 4.Department of Biological ScienceAuburn UniversityAuburnUSA
  5. 5.Department of BiologyRollins CollegeWinter ParkUSA

Personalised recommendations