Advertisement

Estuaries and Coasts

, Volume 41, Issue 3, pp 751–764 | Cite as

Genetic Diversity of Benthic Microbial Eukaryotes in Response to Spatial Heterogeneity of Sediment Geochemistry in a Mangrove Ecosystem

  • Ping Zhu
  • Yaping Wang
  • Tiantian Shi
  • Guoqiang Huang
  • Jun GongEmail author
Article

Abstract

Little is known about the diversity, community composition, or distribution of benthic microbial eukaryotes in organic carbon (OC)-rich mangrove sediments. We hypothesized that the distribution of microeukaryotes was related to the spatial heterogeneity of mangrove sediment geochemistry due to tidal zonation and the rhizosphere effect. A range of geochemical properties of surface sediments were characterized, and alpha and beta diversities of microeukaryotes in a mangrove ecosystem were investigated using MiSeq sequencing of 18S rRNA genes. We found that the sequence proportions of Chlorophyta and Bacillariophyta were notably high in the datasets. Both operational taxonomic unit (OTU) richness and microeukaryotic community structure (MCS) were significantly different between the OC-rich upper tidal zone and the sulfate- and ammonium-rich lower tidal zone, indicating a strong response of microeukaryotic diversity to tidal zonation. The zonewise community differences were characterized by distinct shifts in the proportions and OTUs of chlorophytes, diatoms, and fungi. However, neither OTU richness nor MCS was significantly different between near-root and bulk sediments, though several geochemical parameters varied. Similarly, the assemblages of fungi showed a pattern of tidal zonation. Overall, variations in MCS in mangrove sediments were mainly driven by the quantity and quality of organic matter, grain size, and concentration of sulfate.

Keywords

Biogeochemistry Blue carbon ecosystem Protist Fungi Benthos Rhizosphere effect 

Notes

Acknowledgments

This work was supported by the Natural Science Foundation of China (Nos. 41522604 and 31572255), the Strategic Priority Research Program of CAS (No. XDA11020702), the Science and Technology Development Program of Yantai (No. 2014ZH073), and the Special Program for Basic Research of the Ministry of Science and Technology, China (No. 2014FY210600).

Supplementary material

12237_2017_317_MOESM1_ESM.pdf (516 kb)
ESM 1 (PDF 515 kb)

References

  1. Algeo, T.J., G.M. Luo, H.Y. Song, T.W. Lyons, and D.E. Canfield. 2015. Reconstruction of secular variation in seawater sulfate concentrations. Biogeosciences 12: 2131–2151.CrossRefGoogle Scholar
  2. Alongi, D.M. 2005. Mangrove–microbe–soil relations. In Interactions between macro- and microorganisms in marine sediments, ed. E. Kristensen, R.R. Haese, and J.E. Kostka, 85–103. Washington: American Geophysical Union.CrossRefGoogle Scholar
  3. Alongi, D.M. 2016. Mangroves. In Encyclopedia of estuaries, ed. M.J. Kennish, 393–404. Berlin: Springer Science.CrossRefGoogle Scholar
  4. Alongi, D.M., A. Sasekumar, F. Tirendi, and P. Dixon. 1998. The influence of stand age on benthic decomposition and recycling of organic matter in managed mangrove forests of Malaysia. Journal of Experimental Marine Biology and Ecology 225: 197–218.CrossRefGoogle Scholar
  5. Andersen, F.O., and E. Kristensen. 1988. Oxygen microgradients in the rhizosphere of the mangrove Avicennia marina. Marine Ecology Progress Series 44: 201–204.CrossRefGoogle Scholar
  6. Arfi, Y., C. Marchand, M. Wartel, and E. Record. 2012. Fungal diversity in anoxic-sulfidic sediments in a mangrove soil. Fungal Ecology 5: 282–285.CrossRefGoogle Scholar
  7. Asiloglu, R., H. Honjo, N. Saka, S. Asakawa, and J. Murase. 2015. Community structure of microeukaryotes in a rice rhizosphere revealed by DNA-based PCR-DGGE. Soil Science and Plant Nutrition 61: 761–768.CrossRefGoogle Scholar
  8. Azam, F., T. Fenchel, J.G. Field, J.S. Gray, L.A. Meyer-Reil, and F. Thingstad. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10: 257–263.CrossRefGoogle Scholar
  9. Bagarinao, T. 1992. Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquatic Toxicology 24: 21–62.CrossRefGoogle Scholar
  10. Baldwin, D.S., and A.M. Mitchell. 2000. The effects of drying and re-flooding on the sediment and soil nutrient dynamics of lowland river-floodplain systems: a synthesis. Regulated Rivers: Research and Management 16: 457–467.CrossRefGoogle Scholar
  11. Barnett, A., V. Méléder, L. Blommaert, B. Lepetit, P. Gaudin, et al. 2015. Growth form defines physiological photoprotective capacity in intertidal benthic diatoms. The ISME Journal 9: 32–45.CrossRefGoogle Scholar
  12. Bossio, D.A., J.A. Fleck, K.M. Scow, and R. Fujii. 2006. Alteration of soil microbial communities and water quality in restored wetlands. Soil Biology and Biochemistry 38: 1223–1233.CrossRefGoogle Scholar
  13. Bottrell, S.H., and R.J. Newton. 2006. Reconstruction of changes in global sulfur cycling from marine sulfate isotopes. Earth-Science Reviews 75: 59–83.CrossRefGoogle Scholar
  14. Bouillon, S., T. Moens, I. Overmeer, N. Koedam, and F. Dehairs. 2004. Resource utilization patterns of epifauna from mangrove forests with contrasting inputs of local versus imported organic matter. Marine Ecology Progress Series 278: 77–88.CrossRefGoogle Scholar
  15. Bulman, S.R., S.F. Kühn, J.W. Marshall, and E. Schnepf. 2001. A phylogenetic analysis of the SSU rRNA from members of the Plasmodiophorida and Phagomyxida. Protist 152: 43–51.CrossRefGoogle Scholar
  16. Caporaso, J.G., J. Kuczynski, J. Stombaugh, K. Bittinger, F.D. Bushman, E.K. Costello, and N. Fierer. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335–336.CrossRefGoogle Scholar
  17. Carini, P., P.J. Marsden, J.W. Leff, E.E. Morgan, M.S. Strickland, and N. Fierer. 2016. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nature Microbiology 2: 16242.CrossRefGoogle Scholar
  18. Caron, D.A., P.D. Countway, and M.V. Brown. 2004. The growing contributions of molecular biology and immunology to protistan ecology: Molecular signatures as ecological tools. Journal of Eukaryotic Microbiology 51: 38–48.CrossRefGoogle Scholar
  19. Cartaxana, P., M. Ruivo, C. Hubas, I. Davidson, J. Serȏdio, and B. Jesus. 2011. Physiological versus behavioral photoprotection in intertidal epipelic and epipsammic benthic diatom communities. Journal of Experimental Marine Biology and Ecology 405: 120–127.CrossRefGoogle Scholar
  20. Chambers, L.G., R. Guevara, J.N. Boyer, T.G. Troxler, and S.E. Davis. 2016. Effects of salinity and inundation on microbial community structure and function in a mangrove peat soil. Wetlands 36: 361–371.CrossRefGoogle Scholar
  21. Chariton, A.A., L.N. Court, D.M. Hartley, M.J. Colloff, and C.M. Hardy. 2010. Ecological assessment of estuarine sediments by pyrosequencing eukaryotic ribosomal DNA. Frontiers in Ecology and the Environment 8: 233–238.CrossRefGoogle Scholar
  22. Clarke, K.R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.CrossRefGoogle Scholar
  23. Dazzo, F.B., and S. Gantner. 2012. The rhizosphere. In Topics in ecological and environmental microbiology, ed. T.M. Schmidt and M. Schaechter, 466–480. Massachusetts: Academic Press.Google Scholar
  24. Dell'Anno, A., and C. Corinaldesi. 2004. Degradation and turnover of extracellular DNA in marine sediments: ecological and methodological considerations. Applied and Environmental Microbiology 70: 4384–4386.CrossRefGoogle Scholar
  25. Dittmar, T., N. Hertkorn, G. Kattner, and R.J. Lara. 2006. Mangroves, a major source of dissolved organic carbon to the oceans. Global Biogeochemical Cycles 20: GB1012.CrossRefGoogle Scholar
  26. Drenovsky, R.E., D. Vo, K.J. Graham, and K.M. Scow. 2004. Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microbial Ecology 48: 424–430.CrossRefGoogle Scholar
  27. Edgar, R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.CrossRefGoogle Scholar
  28. Elwood, H.J., G.J. Olsen, and M.L. Sogin. 1985. The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Molecular Biology and Evolution 2: 399–410.Google Scholar
  29. Fenchel, T. 1969. The ecology of marine microbenthos. IV Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna communities with special reference to the ciliated protozoa. Ophelia 6: 1–182.CrossRefGoogle Scholar
  30. Finkel, Z.V., J. Beardall, K.J. Flynn, A. Quigg, T.A.V. Rees, and J.A. Raven. 2010. Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research 32: 119–137.CrossRefGoogle Scholar
  31. Forster, D., M. Dunthorn, F. Mah’e, J.R. Dolan, et al. 2016. Benthic protists: the under-charted majority. FEMS Microbiology Ecology 92: fiw120.CrossRefGoogle Scholar
  32. Fu, R., and J. Gong. 2017. Single cell analysis linking ribosomal (r)DNA and rRNA copy numbers to cell size and growth rate provides insights into molecular protistan ecology. Journal of Eukaryotic Microbiology.  https://doi.org/10.1111/jeu.12425.
  33. Glücksman, E., T. Bell, R.I. Griffiths, and D. Bass. 2010. Closely related protist strains have different grazing impacts on natural bacterial communities. Environmental Microbiology 12: 3105–3113.CrossRefGoogle Scholar
  34. Gomes, N.C.M., D.F.R. Cleary, F.N. Pinto, C. Egas, A. Almeida, et al. 2010. Taking root: enduring effect of rhizosphere bacterial colonization in mangroves. PloS One 5: e14065.CrossRefGoogle Scholar
  35. Gomes, N.C.M., D.F.R. Cleary, A.C.C. Pires, A. Almeida, et al. 2014. Assessing variation in bacterial composition between the rhizospheres of two mangrove tree species. Estuarine, Coastal and Shelf Science 139: 40–45.CrossRefGoogle Scholar
  36. Gong, J., F. Shi, B. Ma, J. Dong, M. Pachiadaki, X.L. Zhang, and V.P. Edgcomb. 2015. Depth shapes α- and β-diversities of microbial eukaryotes in surficial sediments of coastal ecosystems. Environmental Microbiology 17: 3722–3737.CrossRefGoogle Scholar
  37. Gontikaki, E., B. Thornton, T. Cornulier, and U. Witte. 2015. Occurrence of priming in the degradation of lignocellulose in marine sediments. PloS One 10: e0143917.CrossRefGoogle Scholar
  38. Guillou, L., D. Bachar, S. Audic, D. Bass, C. Berney, L. Bittner, et al. 2013. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Research 41: D597–D604.CrossRefGoogle Scholar
  39. Holguin, G., P. Vazquez, and Y. Bashan. 2001. The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biology and Fertility of Soils 33: 265–278.CrossRefGoogle Scholar
  40. Hyde, K.D., E.B.G. Jones, E. Leaño, S.B. Pointing, A.D. Poonyth, and L.L.P. Vrijmoed. 1998. Role of fungi in marine ecosystems. Biodiversity and Conservation 7: 1147–1161.Google Scholar
  41. Jesus, B., V. Brotas, L. Ribeiro, C.R. Mendes, P. Cartaxana, and D.M. Paterson. 2009. Adaptations of microphytobenthos assemblages to sediment type and tidal position. Continental Shelf Research 29: 1624–1634.CrossRefGoogle Scholar
  42. Kirchmair, M., S. Neuhauser, and L. Huber. 2005. Sorosphaera viticola sp. nov. (plasmodiophorids), an intracellular parasite in roots of grape vine. Sydowia 57: 223–232.Google Scholar
  43. Klimek, B., J. Fyda, A. Pajdak-Stós, W. Kocerba, E. Fiałkowska, and M. Sobczyk. 2012. Toxicity of ammonia nitrogen to ciliated protozoa Stentor coeruleus and Coleps hirtus isolated from activated sludge of wastewater treatment plants. Bulletin of Environmental Contamination and Toxicology 89: 975–977.CrossRefGoogle Scholar
  44. Kristensen, E., S. Bouillon, T. Dittmar, and C. Marchand. 2008. Organic carbon dynamics in mangrove ecosystems: A review. Aquatic Botany 89: 201–219.CrossRefGoogle Scholar
  45. Leander, B.S. 2008. Marine gregarines: evolutionary prelude to the apicomplexan radiation. Trends in Parasitology 24: 60–67.CrossRefGoogle Scholar
  46. Leander, B.S., J.T. Harper, and P.J. Keeling. 2003. Molecular phylogeny and surface morphology of marine aseptate gregarines (Apicomplexa): Selenidium spp. and Lecudina spp. Journal of Parasitology 89: 1191–1205.CrossRefGoogle Scholar
  47. Lennon, J.T., S.A. Placella, and M.E. Muscarella. 2017. Relic DNA contributes minimally to estimates of microbial diversity. bioRxiv.  https://doi.org/10.1101/131284.
  48. Manson, F.J., N.R. Loneragan, G.A. Skilleter, and S.R. Phinn. 2005. An evaluation of the evidence for linkages between mangroves and fisheries: a synthesis of the literature and identification of research directions. Oceanography and Marine Biology: An Annual Review 43: 483–513.Google Scholar
  49. Marañón, E., P.M. Holligan, R. Barciela, N. González, et al. 2001. Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments. Marine Ecology Progress Series 216: 43–56.CrossRefGoogle Scholar
  50. Marchand, C., F. Baltzer, E. Lallier-Vergès, and P. Albéric. 2004. Pore-water chemistry in mangrove sediments: relationship with species composition and developmental stages (French Guiana). Marine Geology 208: 361–381.CrossRefGoogle Scholar
  51. Massana, R., A. Gobet, S. Audic, D. Bass, L. Bittner, et al. 2015. Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing. Environmental Microbiology 17: 4035–4049.CrossRefGoogle Scholar
  52. McMurdie, P.J., and S. Holmes. 2014. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Computational Biology 10: e1003531.CrossRefGoogle Scholar
  53. Meyers, P.A. 1994. Preservation of elemental and isotopic source identification of sedimentary organic matter. Chemical Geology 114: 289–302.CrossRefGoogle Scholar
  54. Mitbavkar, S., and A.C. Anil. 2004. Vertical migratory rhythms of benthic diatoms in a tropical intertidal sand flat: Influence of irradiance and tides. Marine Biology 145: 9–20.CrossRefGoogle Scholar
  55. Neatrour, M.A., J.R. Webster, and E.E. Benfield. 2004. The role of floods in particulate organic matter dynamics of a southern Appalachian river-floodplain ecosystem. Journal of the North American Benthological Society 23: 198–213.CrossRefGoogle Scholar
  56. Nedwell, D.B., T.H. Blackburn, and W.J. Wiebe. 1994. Dynamic nature of the turnover of organic carbon, nitrogen and sulphur in the sediments of a Jamaican mangrove forest. Marine Ecology Progress Series 110: 223–231.CrossRefGoogle Scholar
  57. Neuhauser, S., M. Kirchmair, S. Bulman, and D. Bass. 2014. Cross-kingdom host shifts of phytomyxid parasites. BMC Evolutionary Biology. 14: 33.CrossRefGoogle Scholar
  58. Park, S.J., B.J. Park, V.H. Pham, D.N. Yoon, S.K. Kim, and S.K. Rhee. 2008. Microeukaryotic diversity in marine environments, an analysis of surface layer sediments from the East Sea. The Journal of Microbiology 49: 244–249.CrossRefGoogle Scholar
  59. Pires, A.C.C., D.F.R. Cleary, A. Almeida, A. Cunha, S. Dealtry, et al. 2012. Denaturing gradient gel electrophoresis and barcoded pyrosequencing reveal unprecedented archaeal diversity in mangrove sediment and rhizosphere samples. Applied and Environmental Microbiology 78: 5520–5528.CrossRefGoogle Scholar
  60. Reef, R., I.C. Feller, and C.E. Lovelock. 2010. Nutrition of mangroves. Tree Physiology 30: 1148–1160.CrossRefGoogle Scholar
  61. Richards, T.A., M.D.M. Jones, G. Leonard, and D. Bass. 2012. Marine fungi: their ecology and molecular diversity. Annual Review of Marine Science 4: 495–522.Google Scholar
  62. Robinson, M.D., D.J. McCarthy, and G.K. Smyth. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.CrossRefGoogle Scholar
  63. Rysgaard, S., P.B. Christensen, M.V. Sørensen, P. Funch, and P. Berg. 2000. Marine meiofauna, carbon and nitrogen mineralization in sandy and soft sediments of Disko Bay, West Greenland. Aquatic Microbial Ecology 21: 59–71.CrossRefGoogle Scholar
  64. Santos, H.F., J.C. Cury, F.L. Carmo, A.S. Rosado, and R.S. Peixoto. 2010. 18S rDNA sequences from microeukaryotes reveal oil indicators in mangrove sediment. PloS One 5: e12437.CrossRefGoogle Scholar
  65. Schloss, P.D., S.L. Westcott, T. Ryabin, J.R. Hall, M. Hartmann, E.B. Hollister, et al. 2009. Introducing Mothur: open-source, platform-independent, community supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75: 7537–7541.CrossRefGoogle Scholar
  66. Schuur, E.A.G., and P.A. Matson. 2001. Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128: 431–442.CrossRefGoogle Scholar
  67. Sifleet, S., L. Pendleton and B.C. Murray. 2011. State of the science on coastal blue carbon: A summary for policy makers. https://nicholasinstitute.duke.edu/ocean/publications/naturalresources/state-of-science-coastal-blue-carbon. May 2011.
  68. Sun, F., X. Zhang, Q. Zhang, F. Liu, J. Zhang, and J. Gong. 2015. Seagrass (Zostera marina) colonization promotes the accumulation of diazotrophic bacteria and alters the relative abundances of specific bacterial lineages involved in benthic carbon and sulfur cycling. Applied and Environmental Microbiology 81: 6901–6914.CrossRefGoogle Scholar
  69. ter Braak, C.J.F., and P. Smilauer. 2002. CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical ordination, version 4.5. Ithaca: Microcomputer Power.Google Scholar
  70. Torti, A., M.A. Lever, and B.B. Jørgensen. 2015. Origin, dynamics, and implications of extracellular DNA pools in marine sediments. Marine Genomics 24: 185–196.CrossRefGoogle Scholar
  71. Unger, I.M., A.C. Kennedy, and R.M. Muzika. 2009. Flooding effects on soil microbial communities. Applied Soil Ecology 42: 1–8.CrossRefGoogle Scholar
  72. Van Der Wal, A., T.D. Geydan, T.W. Kuyper, and W. de Boer. 2013. A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiology Reviews 37: 477–494.CrossRefGoogle Scholar
  73. Weckström, J., and A. Korhola. 2001. Patterns in the distribution, composition and diversity of diatom assemblages in relation to ecoclimatic factors in Arctic Lapland. Journal of Biogeography 28: 31–45.CrossRefGoogle Scholar
  74. Xu, H., W. Song, L. Lu, and A. Warren. 2005. Tolerance of ciliated protozoan Paramecium bursaria (Protozoa, Ciliophora) to ammonia and nitrites. Chinese Journal of Oceanology and Limnology 23: 349–353.CrossRefGoogle Scholar
  75. Yu, Z., J. Yang, X.Q. Yu, L.M. Liu, and Y. Tian. 2014. Aboveground vegetation influences belowground microeukaryotic community in a mangrove nature reserve. Wetlands 34: 393–401.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  1. 1.Yantai Institute of Coastal Zone ResearchChinese Academy of SciencesYantaiChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Guangxi Institute of OceanologyBeihaiChina
  4. 4.Laboratory of Microbial Ecology and Matter Cycles, School of Marine SciencesSun Yat-Sen UniversityZhuhaiChina

Personalised recommendations