Skip to main content
Log in

Adaptation of Ulva lactuca in low-salinity and high-nutrient water environment and its synergistic microbial effect on inorganic nitrogen removal

  • Research
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Excess inorganic nitrogen in offshore estuarine areas can adversely affect coastal water quality. To explore the bioremediation potential of Ulva lactuca in low-salinity and high-nutrient water, the dissolved inorganic nitrogen (DIN) removal under different low salinities (0, 0.5, 1.0, 1.5, 2.0% NaCl) and high nutrients was studied. Static culture experiments exhibited a maximum DIN removal efficiency of 73.74% with U. lactuca in the 1.0% salinity system. The differences in DIN removal efficiency at 1.0, 1.5 and 2.0% NaCl salinity were not significant (p > 0.05 and could reach above 65%. High-throughput sequencing, scanning electron microscopy (SEM) and excitation emission matrix (EEM) analysis demonstrated that the diversity of microorganisms decreased with increasing salinity with Proteobacteria and Bacteroidota the main phyla, revealing the synergistic effect of U. lactuca and microbes. Response surface curves showed that the conditions affecting DIN removal efficiency from high to low were salinity, density, and C/N ratio. By simulating the fluctuation of salinity and water level in the offshore estuarine environment, the efficient DIN removal was more than 60% and dissolved oxygen (DO) concentration was about 8 mg L−1 with U. lactuca at salinity above 1.0% NaCl. In conclusion, this study explored the DIN removal pattern of U. lactuca in different low-salinity and high-nutrient water environments, which is of great importance for the ecological restoration of estuarine and coastal environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available in the Figshare repository. https://doi.org/10.6084/m9.figshare.24123648.

References

  • APHA (1985) Standard methods for the examination of water and wastewater, 16th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Archin S, Sharifi SH, Asadpour G (2019) Optimization and modeling of simultaneous ultrasound-assisted adsorption of binary dyes using activated carbon from tobacco residues: Response surface methodology. J Clean Prod 239:118136

    CAS  Google Scholar 

  • Arumugam N, Chelliapan S, Kamyab H, Thirugnana S, Othman N, Nasri NS (2018) Treatment of wastewater using seaweed: A review. Int J Environ Res Public Health 15:2851

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bao M, Xing Q, Park JS, He P, Zhang J, Yarish C, Kim JK (2023) Temperature and high nutrients enhance hypo-salinity tolerance of the bloom forming green alga. Ulva Prolifera Harmful Algae 123:102402

    CAS  PubMed  Google Scholar 

  • Bencherif K, Boutekrabt A, Fontaine J, Laruelle F, Dalpè Y, Sahraoui AL (2015) Impact of soil salinity on arbuscular mycorrhizal fungi biodiversity and microflora biomass associated with Tamarix articulata Vahll rhizosphere in arid and semi-arid Algerian areas. Sci Total Environ 533:488–494

    CAS  PubMed  ADS  Google Scholar 

  • Braña V, Cagide C, More, MA (2016) The sustainable use of Delftia in agriculture, bioremediation, and bioproducts synthesis. In: Castro-Sowinski S (ed) Microbial Models: From Environmental to Industrial Sustainability. Microorganisms for Sustainability. Springer, Singapore pp 227–247

  • Bruhn A, Dahl J, Nielsen HB, Nikolaisen L, Rasmussen MB, Markager S, Olesen B, Arias C, Jensen PD (2011) Bioenergy potential of Ulva lactuca: Biomass yield, methane production and combustion. Bioresour Technol 102:2595–2604

    CAS  PubMed  Google Scholar 

  • Chen B, Zou D, Zhu M (2015) Growth and photosynthetic responses of Ulva lactuca (Ulvales, Chlorophyta) germlings to different pH levels. Mar Biol Res 13:351–357

    Google Scholar 

  • Chen H, Wang Y, Chen Z, Wu Z, Chu X, Qing S, Xu L, Yang K, Meng Q, Cheng H, Zhan W, Wang Y, Zhou H (2023) Effects of salinity on anoxic–oxic system performance, microbial community dynamics and co-occurrence network during treating wastewater. Chem Eng J 461:141969

    CAS  Google Scholar 

  • Chi Z, Zhu Y, Li H, Wu H, Yan B (2021) Unraveling bacterial community structure and function and their links with natural salinity gradient in the Yellow River Delta. Sci Total Environ 773:145673

    CAS  PubMed  ADS  Google Scholar 

  • Coble PG (1996) Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Mar Chem 51:325–346

    CAS  Google Scholar 

  • Deniz F, Ersanli ET (2017) An ecofriendly approach for bioremediation of contaminated water environment: Potential contribution of a coastal seaweed community to environmental improvement. Int J Phytorem 20:256–263

    Google Scholar 

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929

    CAS  PubMed  ADS  Google Scholar 

  • Fabre E, Vale C, Pereira E, Silva CM (2019) Experimental measurement and modeling of Hg(II) removal from aqueous solutions using Eucalyptus globulus Bark: Effect of pH, salinity and biosorbent dosage. Int J 20(23):5973

    Google Scholar 

  • Ferreira N, Viana T, Henriques B, Tavares DS, Jacinto J, Colónia J, Pinto J, Pereira E (2023) Application of response surface methodology and Box-Behnken design for the optimization of mercury removal by Ulva sp. J Hazard Mat 445:130405

    CAS  Google Scholar 

  • Fu G, Zhao L, Huangshen L, Wu J (2019) Isolation and identification of a salt-tolerant aerobic denitrifying bacterial strain and its application to saline wastewater treatment in constructed wetlands. Bioresour Technol 290:121725

    CAS  PubMed  Google Scholar 

  • Gao Y, Wang X, Li J, Lee CT, Ong PY, Zhang Z, Li C (2020) Effect of aquaculture salinity on nitrification and microbial community in moving bed bioreactors with immobilized microbial granules. Bioresour Technol 297:122427

    CAS  PubMed  Google Scholar 

  • Hu YSU (2023) Opportunity and challenges of phenotyping plant salt tolerance. Trends Plant Sci 28:552–566

    CAS  PubMed  Google Scholar 

  • Jia L, Liu H, Kong Q, Li M, Wu S, Wu H (2019) Interactions of high-rate nitrate reduction and heavy metal mitigation in iron-carbon-based constructed wetlands for purifying contaminated groundwater. Water Res 169:115285

    PubMed  Google Scholar 

  • Jones DR (2001) A taxonomy of global optimization methods based on response surfaces. J Glob Optim 21:345–383

    MathSciNet  Google Scholar 

  • Kim S-K (ed) (2015) Springer Handbook of Marine Biotechnology. Springer, Dordrecht

    Google Scholar 

  • Kim J-H, Kang EJ, Park MG, Lee B-G, Kim KY (2011) Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea. J Appl Phycol 23:421–432

    Google Scholar 

  • Lananan F, Hamid SHA, Din WNS, Ali N, Khatoon H, Jusoh A, Endut A (2014) Symbiotic bioremediation of aquaculture wastewater in reducing ammonia and phosphorus utilizing Effective Microorganism (EM-1) and microalgae (Chlorella sp.). Int Biodeterior Biodegrad 95:127–134

    CAS  Google Scholar 

  • Long Y, Ma Y, Wan J, Wang Y, Tang M, Fu H, Cao J (2023a) Denitrification efficiency, microbial communities and metabolic mechanisms of corn cob hydrolysate as denitrifying carbon source. Environ Res 221:115315

    CAS  PubMed  Google Scholar 

  • Long Y, Ma Y, Wan J, Wang Y, Thang M, Zheng Q, Ma Y (2023b) Hydrolysate from the enzymatic treatment of corn cob as a carbon source for heterotrophic denitrification process. J Water Process Eng 51:103473

    Google Scholar 

  • Mantri VA, Kazi MA, Balar NB, Gupta V, Gajaria T (2020) Concise review of green algal genus Ulva Linnaeus. J Appl Phycol 32:2725–2741

    Google Scholar 

  • Mirazimi SMJ, Rashchi F, Saba M (2013) Vanadium removal from roasted LD converter slag: Optimization of parameters by response surface methodology (RSM). Sep Purif Technol 116:175–183

    CAS  Google Scholar 

  • Msuya F, Kyewalanga MS, Salum D (2006) The performance of the seaweed Ulva reticulata as a biofilter in a low-tech, low-cost, gravity generated water flow regime in Zanzibar, Tanzania. Aquaculture 254:284–292

    Google Scholar 

  • Nederlof MAJ, Neori A, Verdegem MCJ, Smaal AC, Jansen HM (2022) Ulva spp. performance and biomitigation potential under high nutrient concentrations: implications for recirculating IMTA systems. J Appl Phycol 34 (4):2157–2171

  • Neveux N, Bolton JJ, Bruhn A, Roberts TA, Ras M (2018) The bioremediation potential of seaweeds: Recycling nitrogen, phosphorus, and other waste products. In: La Barre S, Bates SS (eds) Blue Biotechnology, vol 1. Wiley-VCH, Weinheim, pp 217–237

    Google Scholar 

  • Nikolaisen L, Daugbjerg Jensen P, SvaneBech K, Dahl J, Busk J, Brødsgaard T, Rasmussen MB, Bruhn A, Bjerre A-B, Bangsø Nielsen H, Albert KR, Ambus P, Kádár Z, Heiske S, Sander B, Bruhn A, Bjerre A-B, Bangsø Nielsen H, Albert KR, Ambus P, Kádár Z, Heiske S, Sander B, Schmidt ER (2011) Energy Production from Marine Biomass (Ulva lactuca). Danish Technological Institute, Taastrup, Denmark

    Google Scholar 

  • Normant M, Lamprecht I (2006) Does scope for growth change as a result of salinity stress in the amphipod Gammarus oceanicus? J Exp Mar Biol Ecol 334:158–163

    Google Scholar 

  • Park D, Yun Y-S, Park JM (2010) The past, present, and future trends of biosorption. Biotechnol Bioprocess Eng 15:86–102

    CAS  Google Scholar 

  • Passatore L, Rossetti S, Juwarkar AA, Massacci A (2014) Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): State of knowledge and research perspectives. J Hazard Mat 278:189–202

  • Pedersen MF, Paling EI, Walker DI (1997) Nitrogen uptake and allocation in the seagrass Amphibolis antarctica. Aquat Bot 56:105–117

    CAS  Google Scholar 

  • Peng CL, Wen X, Lin Z-F, Zhou H-C, Chen S-W, Lin G-Z (2007) Response of Gracilaria lemaneiformis to nitrogen and phosphorus eutrophic seawater. J Plant Ecol 31:505–512 (In Chinese)

    CAS  Google Scholar 

  • Raman DR, Spanswick RM, Walker LP (1995) The kinetics of nitrate uptake from flowing solutions by rice: Influences of pretreatment nitrate concentration and irradiance. Bioresour Technol 53:125–132

    CAS  Google Scholar 

  • Revilla-Lovano S, Sandoval-Gil JM, Zertuche-González JA, Belando-Torrentes MD, Bernardeau-Esteller J, Rangel-Mendoza LK, Ferreira-Arrieta A, Guzmán-Calderón JM, Camacho-Ibar VF, Muñiz-Salazar R, Ávila-López MdC (2021) Physiological responses and productivity of the seaweed Ulva ohnoi (Chlorophyta) under changing cultivation conditions in pilot large land-based ponds. Algal Res 56:102316

    Google Scholar 

  • She Z, Zhao L, Zhang X, Jin C, Guo L, Yang S, Zhao Y, Gao M (2016) Partial nitrification and denitrification in a sequencing batch reactor treating high-salinity wastewater. Chem Eng J 288:207–215

    CAS  Google Scholar 

  • Skriptsova AV, Miroshnokova NV (2011) Laboratory experiment to determine the potential of two macroalgae from the Russian Far-East as biofilters for integrated multi-trophic aquaculture (IMTA). Bioresour Technol 102:3149–3154

    CAS  PubMed  Google Scholar 

  • Sode S, Bruhn A, Balsby TJ, Larsen MM, Gotfredsen A, Rasmussen MB (2013) Bioremediation of reject water from anaerobically digested waste water sludge with macroalgae (Ulva lactuca, Chlorophyta). Bioresour Technol 146:426–435

    CAS  PubMed  Google Scholar 

  • Venkataramana V, Garade L, Bharathi MD, Sarma VVSS (2023) Role of salinity on zooplankton assemblages in the tropical Indian estuaries during post monsoon. Mar Poll Bull 190:114816

    CAS  Google Scholar 

  • Wang H, Liu C-F, Qin C-X, Cao S-Q, Ding J (2007) Using a macroalgae Ulva pertusa biofilter in a recirculating system for production of juvenile sea cucumber Apostichopus japonicus. Aquacult Eng 36:217–224

    Google Scholar 

  • Wang X, Chen RF, Cable JE, Cherrier J (2014) Leaching and microbial degradation of dissolved organic matter from salt marsh plants and seagrasses. Aquat Sci 76:595–609

    Google Scholar 

  • Wang X, Zhu H, Yan B, Shutes B, Bañuelos G, Wen H (2020) Bioaugmented constructed wetlands for denitrification of saline wastewater: A boost for both microorganisms and plants. Environ Int 138:105628

    CAS  PubMed  Google Scholar 

  • Wang Z, Gao M, She Z, Wang S, Jin C, Zhao Y, Yang S, Guo L (2015) Effects of salinity on performance, extracellular polymeric substances and microbial community of an aerobic granular sequencing batch reactor. Sep Purif Technol 144:223–231

    CAS  Google Scholar 

  • Williams JB, May E, Ford MG, Butler JE (1994) Nitrogen transformations in gravel bed hydroponic beds used as a tertiary treatment stage for sewage effluents. Water Sci Technol 29:29–36

    CAS  Google Scholar 

  • Xia Z, Liu G, She Z, Gao M, Zhao Y, Guo L, Jin C (2020) Performance and bacterial communities in unsaturated and saturated zones of a vertical-flow constructed wetland with continuous-feed. Bioresour Technol 315:123859

    CAS  PubMed  Google Scholar 

  • Xu S, Yu Z, Zhou Y, Yue S, Liang J, Zhang X (2023) The potential for large-scale kelp aquaculture to counteract marine eutrophication by nutrient removal. Mar Pollut Bull 187:114513

    CAS  PubMed  Google Scholar 

  • Yu Y, Zhang H, Lemckert C (2014) Salinity and turbidity distributions in the Brisbane River estuary, Australia. J Hydrol 519:3338–3352

    Google Scholar 

  • Zeraatkar AK, Ahmadzadeh H, Talebi AF, Moheimani NR, McHenry MP (2016) Potential use of algae for heavy metal bioremediation, a critical review. J Environ Manage 181:817–831

    CAS  PubMed  Google Scholar 

  • Zhang T, Wang X (2017) Release and microbial degradation of dissolved organic matter (DOM) from the macroalgae Ulva prolifera. Mar Pollut Bull 125:192–198

    CAS  PubMed  Google Scholar 

  • Xiao J, Zhang X, Gao C, Jiang M, Li R, Wang Z, Li Y, Fan S, Zhang X (2016) Effect of temperature, salinity and irradiance on growth and photosynthesis of Ulva prolifera. Acta Oceanol Sin 35:114–121

    Article  CAS  Google Scholar 

  • Zhao L, Xin P, Cheng H, Cho A (2022) Combined effects of river discharge regulation and estuarine morphological evolution on salinity dynamics in Yangtze Estuary, China. Estuar Coast Shelf Sci 276:108002

    CAS  Google Scholar 

  • Zheng L, Dong Y, Li B, Yin T, Liu C, Lin H (2022) Simultaneous removal of high concentrations of ammonia nitrogen and calcium by the novel strain Paracoccus denitrificans AC-3 with good environmental adaptability. Bioresour Technol 359:127457

    CAS  PubMed  Google Scholar 

  • Zhou Q, Li R, Li T, Zhou R, Hou Z, Zhang X (2023) Interactions among microorganisms functionally active for electron transfer and pollutant degradation in natural environments. Eco-Environ Health 2:3–15

    PubMed  PubMed Central  Google Scholar 

  • Zollmann M, Traugott H, Chemodanov A, Liberzon A, Golberg A (2018) Exergy efficiency of solar energy conversion to biomass of green macroalgae Ulva (Chlorophyta) in the photobioreactor. Energy Convers Manage 167:125–133

    Google Scholar 

Download references

Funding

This study was supported by the Guangdong Special Support Program Project (No. 2021JC060580), and the Foshan Science and Technology Innovation Project of Guangdong Province (No. 2130218003140).

Author information

Authors and Affiliations

Authors

Contributions

Jinxin Chen: Experimental conception and completion, Data analysis and interpretation, Writing – original draft. Changzheng Wu: Supervision, Funding support, Writing – review & editing. Jinquan Wan: Supervision, Methodology, Final approval, Writing – review & editing. Yan Wang: Critical revision, Writing – review & editing. Bin Zhu: Formal analysis, Writing – review & editing. Xuejian Wang: Investigation. Zhangqing Bi: Investigation.

Corresponding author

Correspondence to Jinquan Wan.

Ethics declarations

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 30 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, J., Wu, C., Wan, J. et al. Adaptation of Ulva lactuca in low-salinity and high-nutrient water environment and its synergistic microbial effect on inorganic nitrogen removal. J Appl Phycol 36, 513–525 (2024). https://doi.org/10.1007/s10811-023-03121-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-023-03121-w

Keywords

Navigation