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Effects of Aeration on the Formation of Arbuscular Mycorrhiza under a Flooded State and Copper Oxide Nanoparticle Removal in Vertical Flow Constructed Wetlands

  • Environmental Microbiology
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Abstract

In this study, six vertical flow constructed wetlands (VFCWs) planted with Phragmites australis were operated at different aeration times (4 h day−1 and 8 h day−1), aeration modes (continuous and intermittent), and arbuscular mycorrhizal fungi (AMF) inoculation treatments (inoculation with Rhizophagus intraradices and no inoculation) to explore the effects of different aeration strategies on the formation of arbuscular mycorrhiza under a flooded state in VFCWs. In addition, these VFCWs were further used to treat copper oxide nanoparticle (CuO-NP) wastewater to evaluate the correlations among aeration, colonization, growth, and CuO-NP removal. The highest AMF 28S copy number (1.99×105) and colonization in reed roots, with values of 67%, 21%, and 1% for frequency (F%), intensity (M%), and arbuscule abundance (A%), were observed in the treatment with intermittent aeration for 4 h day−1. Aeration significantly increased the dissolved oxygen (DO) concentration and AMF colonization in VFCWs, thereby promoting plant growth and the purification of the CuO-NPs. However, excessive and continuous aeration had little positive effect on AMF colonization. This study provides a theoretical basis for the application of AMF for improving pollutant removal performance in constructed wetlands.

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References

  1. Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic press

  2. Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, Oldroyd GED, Eastmond PJ (2017) Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356(6343):1175. https://doi.org/10.1126/science.aan0081

    Article  CAS  PubMed  Google Scholar 

  3. Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front. Plant Sci. 10:470–470. https://doi.org/10.3389/fpls.2019.00470

    Article  PubMed  PubMed Central  Google Scholar 

  4. Li J, Meng B, Chai H, Yang X, Song W, Li S, Lu A, Zhang T, Sun W (2019) Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Front. Plant Sci. 10:499. https://doi.org/10.3389/fpls.2019.00499

    Article  PubMed  PubMed Central  Google Scholar 

  5. Mathur S, Tomar RS, Jajoo A (2019) Arbuscular mycorrhizal fungi (AMF) protects photosynthetic apparatus of wheat under drought stress. Photosynth. Res. 139(1):227–238. https://doi.org/10.1007/s11120-018-0538-4

    Article  CAS  PubMed  Google Scholar 

  6. Fester T (2013) Arbuscular mycorrhizal fungi in a wetland constructed for benzene-, methyl tert-butyl ether-and ammonia-contaminated groundwater bioremediation. Microb. Biotechnol. 6(1):80–84. https://doi.org/10.1111/j.1751-7915.2012.00357.x

    Article  CAS  PubMed  Google Scholar 

  7. Ramírez-Viga TK, Aguilar R, Castillo-Argüero S, Chiappa-Carrara X, Guadarrama P, Ramos-Zapata J (2018) Wetland plant species improve performance when inoculated with arbuscular mycorrhizal fungi: a meta-analysis of experimental pot studies. Mycorrhiza 28(5):477–493. https://doi.org/10.1007/s00572-018-0839-7

    Article  PubMed  Google Scholar 

  8. Xu ZY, Ban YH, Jiang YH, Zhang XL, Liu XY (2016) Arbuscular mycorrhizal fungi in wetland habitats and their application in constructed wetland: a review. Pedosphere 26(5):592–617. https://doi.org/10.1016/s1002-0160(15)60067-4

    Article  Google Scholar 

  9. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320(1–2):37–77. https://doi.org/10.1007/s11104-008-9877-9

    Article  CAS  Google Scholar 

  10. Fusconi A, Mucciarelli M (2018) How important is arbuscular mycorrhizal colonization in wetland and aquatic habitats? Environ. Exp. Bot. 155:128–141. https://doi.org/10.1016/j.envexpbot.2018.06.016

    Article  Google Scholar 

  11. Treseder KK (2013) The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371(1):1–13. https://doi.org/10.1007/s11104-013-1681-5

    Article  CAS  Google Scholar 

  12. Sielaff AC, Polley HW, Fuentes-Ramirez A, Hofmockel K, Wilsey BJ (2019) Mycorrhizal colonization and its relationship with plant performance differs between exotic and native grassland plant species. Bio Invasions 21(6):1981–1991. https://doi.org/10.1007/s10530-019-01950-w

    Article  Google Scholar 

  13. Augé RM, Toler HD, Saxton AM (2014) Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front. Plant Sci. 5:562. https://doi.org/10.3389/fpls.2014.00562

    Article  PubMed  PubMed Central  Google Scholar 

  14. Gunathilakae N, Yapa N, Hettiarachchi R (2018) Effect of arbuscular mycorrhizal fungi on the cadmium phytoremediation potential of Eichhornia crassipes (Mart.) Solms. Groundw. Sustain. Dev. 7:477–482. https://doi.org/10.1016/j.gsd.2018.03.008

    Article  Google Scholar 

  15. Xu ZY, Wu Y, Jiang YH, Zhang XL, Li JL, Ban YH (2018) Arbuscular mycorrhizal fungi in two vertical-flow wetlands constructed for heavy metal-contaminated wastewater bioremediation. Environ. Sci. Pollut. Res. 25(13):12830–12840. https://doi.org/10.1007/s11356-018-1527-z

    Article  CAS  Google Scholar 

  16. Elhindi KM, Al-Mana FA, El-Hendawy S, Al-Selwey WA, Elgorban AM (2018) Arbuscular mycorrhizal fungi mitigates heavy metal toxicity adverse effects in sewage water contaminated soil on Tagetes erecta L. Soil Sci. Plant Nutr. 64(5):662–668. https://doi.org/10.1080/00380768.2018.1490631

    Article  CAS  Google Scholar 

  17. Gomes T, Chora S, Pereira CG, Cardoso C, Bebianno MJ (2014) Proteomic response of mussels Mytilus galloprovincialis exposed to CuO NPs and Cu2+: an exploratory biomarker discovery. Aquat. Toxicol. 155:327–336. https://doi.org/10.1016/j.aquatox.2014.07.015

    Article  CAS  PubMed  Google Scholar 

  18. Dimkpa CO, Latta DE, McLean JE, Britt DW, Boyanov MI, Anderson AJ (2013) Fate of CuO and ZnO nano- and microparticles in the plant environment. Environ Sci Technol 47(9):4734–4742. https://doi.org/10.1021/es304736y

    Article  CAS  PubMed  Google Scholar 

  19. Perreault F, Samadani M, Dewez D (2014) Effect of soluble copper released from copper oxide nanoparticles solubilisation on growth and photosynthetic processes of Lemna gibba L. Nanotoxicology 8(4):374–382. https://doi.org/10.3109/17435390.2013.789936

    Article  CAS  PubMed  Google Scholar 

  20. Buffet PE, Tankoua OF, Pan JF, Berhanu D, Herrenknecht C, Poirier L, Amiard Triquet C, Amiard JC, Bérard JB, Risso C, Guibbolini M, Roméo M, Reip P, Valsami Jones E, Mouneyrac C (2011) Behavioural and biochemical responses of two marine invertebrates Scrobicularia plana and Hediste diversicolor to copper oxide nanoparticles. Chemosphere 84(1):166–174. https://doi.org/10.1016/j.chemosphere.2011.02.003

    Article  CAS  PubMed  Google Scholar 

  21. Zhang HH, Yan MM, Huang TL, Huang X, Yang SY, Li N, Wang N (2020) Water-lifting aerator reduces algal growth in stratified drinking water reservoir: novel insights into algal metabolic profiling and engineering applications. Environ. Pollut. 266:115384. https://doi.org/10.1016/j.envpol.2020.115384

    Article  CAS  PubMed  Google Scholar 

  22. Ćurković L, Cerjan-Stefanović Š, Filipan T (1997) Metal ion exchange by natural and modified zeolites. Water Res. 31(6):1379–1382. https://doi.org/10.1016/S0043-1354(96)00411-3

    Article  Google Scholar 

  23. Dyer A (1988) An introduction to zeolite molecular sieves. John Wiley and Sons Inc, New York

    Google Scholar 

  24. Wu SL, Zhang X, Chen BD, Wu ZX, Li T, Hu YJ, Sun YQ, Wang YS (2016) Chromium immobilization by extraradical mycelium of arbuscular mycorrhiza contributes to plant chromium tolerance. Environ. Exp. Bot. 122:10–18. https://doi.org/10.1016/j.envexpbot.2015.08.006

    Article  CAS  Google Scholar 

  25. Howden R, Cobbett CS (1992) Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol. 100(1):100. https://doi.org/10.1104/pp.100.1.100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J. Hazard. Mater. 154(1):914–926. https://doi.org/10.1016/j.jhazmat.2007.10.121

    Article  CAS  PubMed  Google Scholar 

  27. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55(1):158–IN118. https://doi.org/10.1016/S0007-1536(70)80110-3

    Article  Google Scholar 

  28. Trouvelot A, Kough J (1986) Gianinazzi-Pearson V Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de méthode d'estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and Genetical aspects of mycorrhizae. INRA Press, Paris, pp 217–221

    Google Scholar 

  29. Alkan N, Gadkar V, Coburn J, Yarden O, Kapulnik Y (2004) Quantification of the arbuscular mycorrhizal fungus Glomus intraradices in host tissue using real-time polymerase chain reaction. New Phytol. 161(3):877–885. https://doi.org/10.1046/j.1469-8137.2004.00975.x

    Article  CAS  PubMed  Google Scholar 

  30. Wei FS, Qi WQ, Sun ZG, Huang YR, Shen YW (2002) Water and wastewater monitoring and analysis method. China environmental. Science Press, Beijing

    Google Scholar 

  31. Connell EL, Colmer TD, Walker DI (1999) Radial oxygen loss from intact roots of Halophila ovalis as a function of distance behind the root tip and shoot illumination. Aquat. Bot. 63(3):219–228. https://doi.org/10.1016/S0304-3770(98)00126-0

    Article  Google Scholar 

  32. Tanaka N, Yutani K, Aye T, Jinadasa KBSN (2007) Effect of broken dead culms of Phragmites australis on radial oxygen loss in relation to radiation and temperature. Hydrobiologia 583(1):165–172. https://doi.org/10.1007/s10750-006-0483-7

    Article  CAS  Google Scholar 

  33. Huang J, Wang SH, Yan L, Zhong QS (2010) Plant photosynthesis and its influence on removal efficiencies in constructed wetlands. Ecol. Eng. 36(8):1037–1043. https://doi.org/10.1016/j.ecoleng.2010.04.016

    Article  Google Scholar 

  34. Armstrong J, Afreen-Zobayed F, Blyth S, Armstrong W (1999) Phragmites australis: effects of shoot submergence on seedling growth and survival and radial oxygen loss from roots. Aquat. Bot. 64(3):275–289. https://doi.org/10.1016/S0304-3770(99)00056-X

    Article  Google Scholar 

  35. Dong C, Zhu W, Gao M, Zhao LF, Huang JY, Zhao YQ (2011) Diurnal fluctuations in oxygen release from roots of Acorus calamus Linn in a modeled constructed wetland. J Environ Sci Health, Part A 46(3):224–229. https://doi.org/10.1080/10934529.2011.535391

    Article  CAS  Google Scholar 

  36. Tacon FL, Skinner FA, Mosse B (1983) Spore germination and hyphal growth of a vesicular–arbuscular mycorrhizal fungus, Glomus mosseae (Gerdemann and Trappe), under decreased oxygen and increased carbon dioxide concentrations. Can. J. Microbiol. 29(10):1280–1285. https://doi.org/10.1139/m83-200

    Article  Google Scholar 

  37. Cooke JC, Butler RH, Madole G (1993) Some observations on the vertical distribution of vesicular arbuscular mycorrhizae in roots of salt marsh grasses growing in saturated soils. Mycologia 85(4):547–550. https://doi.org/10.1080/00275514.1993.12026307

    Article  Google Scholar 

  38. Peat HJ, Fitter AH (1993) The distribution of arbuscular mycorrhizas in the British flora. New Phytol. 125(4):845–854. https://doi.org/10.1111/j.1469-8137.1993.tb03933.x

    Article  CAS  PubMed  Google Scholar 

  39. Ipsilantis I, Sylvia DM (2007) Interactions of assemblages of mycorrhizal fungi with two Florida wetland plants. Appl. Soil Ecol. 35(2):261–271. https://doi.org/10.1016/j.apsoil.2006.09.003

    Article  Google Scholar 

  40. Wang YT, Li YW, Bao XZ, Björn LO, Li SS, Olsson PA (2016) Response differences of arbuscular mycorrhizal fungi communities in the roots of an aquatic and a semiaquatic species to various flooding regimes. Plant Soil 403(1):361–373. https://doi.org/10.1007/s11104-016-2811-7

    Article  CAS  Google Scholar 

  41. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17(12):3489. https://doi.org/10.1105/tpc.105.035410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Berthelot C, Blaudez D, Beguiristain T, Chalot M, Leyval C (2018) Co-inoculation of Lolium perenne with Funneliformis mosseae and the dark septate endophyte Cadophora sp. in a trace element-polluted soil. Mycorrhiza 28(3):301–314. https://doi.org/10.1007/s00572-018-0826-z

    Article  CAS  PubMed  Google Scholar 

  43. Roger A, Colard A, Angelard C, Sanders IR (2013) Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence. ISME J 7(11):2137–2146. https://doi.org/10.1038/ismej.2013.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Isayenkov S, Fester T, Hause B (2004) Rapid determination of fungal colonization and arbuscule formation in roots of Medicago truncatula using real-time (RT) PCR. J. Plant Physiol. 161(12):1379–1383. https://doi.org/10.1016/j.jplph.2004.04.012

    Article  CAS  PubMed  Google Scholar 

  45. Gamper HA, Young JP, Jones DL, Hodge A (2008) Real-time PCR and microscopy: are the two methods measuring the same unit of arbuscular mycorrhizal fungal abundance? Fungal Genet. Biol. 45(5):581–596. https://doi.org/10.1016/j.fgb.2007.09.007

    Article  CAS  PubMed  Google Scholar 

  46. Amir H, Cavaloc Y, Laurent A, Pagand P, Gunkel P, Lemestre M, Medevielle V, Pain A, McCoy S (2019) Arbuscular mycorrhizal fungi and sewage sludge enhance growth and adaptation of Metrosideros laurifolia on ultramafic soil in New Caledonia: a field experiment. Sci. Total Environ. 651(Pt 1):334–343. https://doi.org/10.1016/j.scitotenv.2018.09.153

    Article  CAS  PubMed  Google Scholar 

  47. Eskandari S, Guppy CN, Knox OGG, Backhouse D, Haling RE (2017) Mycorrhizal colonisation of cotton in soils differing in sodicity. Pedobiologia 61:25–32. https://doi.org/10.1016/j.pedobi.2017.01.003

    Article  Google Scholar 

  48. Xu ZY, Wu Y, Xiao Z, Ban YH, Belvett N (2019) Positive effects of Funneliformis mosseae inoculation on reed seedlings under water and TiO2 nanoparticles stresses. World J. Microbiol. Biotechnol. 35(6):81. https://doi.org/10.1007/s11274-019-2656-3

    Article  CAS  PubMed  Google Scholar 

  49. Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ. Microbiol. 15(6):1870–1881. https://doi.org/10.1111/1462-2920.12081

    Article  CAS  PubMed  Google Scholar 

  50. Huang XC, Wang L, Ma F (2017) Arbuscular mycorrhizal fungus modulates the phytotoxicity of cd via combined responses of enzymes, thiolic compounds, and essential elements in the roots of Phragmites australis. Chemosphere 187:221–229. https://doi.org/10.1016/j.chemosphere.2017.08.021

    Article  CAS  PubMed  Google Scholar 

  51. Solís-Domínguez FA, Valentín-Vargas A, Chorover J, Maier RM (2011) Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci. Total Environ. 409(6):1009–1016. https://doi.org/10.1016/j.scitotenv.2010.11.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cheng SP, Grosse W, Karrenbrock F, Thoennessen M (2002) Efficiency of constructed wetlands in decontamination of water polluted by heavy metals. Ecol. Eng. 18(3):317–325. https://doi.org/10.1016/S0925-8574(01)00091-X

    Article  Google Scholar 

  53. Wu SL, Zhang X, Sun YQ, Wu ZX, Li T, Hu YJ, Lv JT, Li G, Zhang ZS, Zhang J, Zheng LR, Zhen XJ, Chen BD (2016) Chromium immobilization by extra- and intraradical fungal structures of arbuscular mycorrhizal symbioses. J. Hazard. Mater. 316:34–42. https://doi.org/10.1016/j.jhazmat.2016.05.017

    Article  CAS  PubMed  Google Scholar 

  54. Rask KA, Johansen JL, Kjøller R, Ekelund F (2019) Differences in arbuscular mycorrhizal colonisation influence cadmium uptake in plants. Environ. Exp. Bot. 162:223–229. https://doi.org/10.1016/j.envexpbot.2019.02.022

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by National Natural Science Foundation of China (31800420, 31670541), Natural Science Foundation of Hubei Province (2018CFB126), and the the Fundamental Research Funds for the Central Universities (WUT: 2019IVB046, 2020IB029).

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  1. School of Civil Engineering and Architecture, Wuhan University of Technology, Wuhan, 430070, Hubei, China

    Zhouying Xu, Chen Wu, Yichao Lv & Fake Meng

  2. School of Chemistry, Chemical Engineering and Life Sciences, Wuhan University of Technology, Wuhan, 430070, Hubei, China

    Yihui Ban

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Correspondence to Yihui Ban.

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Xu, Z., Wu, C., Lv, Y. et al. Effects of Aeration on the Formation of Arbuscular Mycorrhiza under a Flooded State and Copper Oxide Nanoparticle Removal in Vertical Flow Constructed Wetlands. Microb Ecol 81, 922–931 (2021). https://doi.org/10.1007/s00248-020-01637-z

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