Engineering microalgae for water phosphorus recovery to close the phosphorus cycle

As a finite and non-renewable resource, phosphorus (P) is essential to all life and crucial for crop growth and food production. The boosted agricultural use and associated loss of P to the aquatic environment are increasing environmental pollution, harming ecosystems, and threatening future global food security. Thus, recovering and reusing P from water bodies is urgently needed to close the P cycle. As a natural, eco-friendly, and sustainable reclamation strategy, microalgae-based biological P recovery is considered a promising solution. However, the low P-accumulation capacity and P-removal efficiency of algal bioreactors restrict its application. Herein, it is demonstrated that manipulating genes involved in cellular P accumulation and signalling could triple the Chlamydomonas P-storage capacity to ~7% of dry biomass, which is the highest P concentration in plants to date. Furthermore, the engineered algae could recover P from wastewater almost three times faster than the unengineered one, which could be directly used as a P fertilizer. Thus, engineering genes involved in cellular P accumulation and signalling in microalgae could be a promising strategy to enhance P uptake and accumulation, which have the potential to accelerate the application of algae for P recovery from the water body and closing the P cycle.

[1]  L. Nussaume,et al.  Cracking the code of plant central phosphate signaling. , 2022, Trends in plant science.

[2]  Xianqing Jia,et al.  Revealing the underlying molecular basis of phosphorus recycling in the green manure crop Astragalus sinicus , 2022, Journal of Cleaner Production.

[3]  J. Sardans,et al.  The global nitrogen-phosphorus imbalance , 2022, Science.

[4]  Houqing Zeng,et al.  Insights of intra/intercellular phosphate transport and signaling in unicellular green algae and multicellular land plants. , 2021, The New phytologist.

[5]  R. Willows,et al.  Bilin-dependent regulation of chlorophyll biosynthesis by GUN4 , 2021, Proceedings of the National Academy of Sciences.

[6]  N. Nirmalakhandan,et al.  Techno-economic optimization of phosphorous recovery in an algal-based sewage treatment system. , 2021, Bioresource technology.

[7]  Yuanda Song,et al.  Microbes as Biofertilizers, a Potential Approach for Sustainable Crop Production , 2021, Sustainability.

[8]  L. Dolan,et al.  Loss of two families of SPX domain-containing proteins required for vacuolar polyphosphate accumulation coincides with the transition to phosphate storage in green plants. , 2021, Molecular plant.

[9]  Seyedeh Fatemeh Mohsenpour,et al.  Integrating micro-algae into wastewater treatment: A review. , 2021, The Science of the total environment.

[10]  Shenmin Zhang,et al.  Current progress, challenges and perspectives in microalgae-based nutrient removal for aquaculture waste: A comprehensive review , 2020 .

[11]  S. B. Faustino,et al.  Floating aquatic macrophytes for the treatment of aquaculture effluents , 2020, Environmental Science and Pollution Research.

[12]  Yiyong Zhu,et al.  Genome-Wide Identification, Expression Profiling, and Evolution of Phosphate Transporter Gene Family in Green Algae , 2020, Frontiers in Genetics.

[13]  Guoliang Zhang,et al.  Application of encapsulated algae into MBR for high-ammonia nitrogen wastewater treatment and biofouling control. , 2020, Water research.

[14]  H. Lambers,et al.  Tightening the Phosphorus Cycle through Phosphorus-Efficient Crop Genotypes. , 2020, Trends in plant science.

[15]  J. Dolfing,et al.  Using Microbial Aggregates to Entrap Aqueous Phosphorus. , 2020, Trends in biotechnology.

[16]  P. Withers Closing the phosphorus cycle , 2019, Nature Sustainability.

[17]  Paul Chen,et al.  Microalgae-based wastewater treatment for nutrients recovery: A review. , 2019, Bioresource technology.

[18]  Robert E. Jinkerson,et al.  A genome-wide algal mutant library and functional screen identifies genes required for eukaryotic photosynthesis , 2019, Nature Genetics.

[19]  Pengcheng Fu,et al.  Algal Biofertilizers and Plant Growth Stimulants for Sustainable Agriculture , 2018, Industrial Biotechnology.

[20]  S. Sugiura Phosphorus, Aquaculture, and the Environment , 2018 .

[21]  J. Elser,et al.  Carbon:Nitrogen:Phosphorus Stoichiometry in Fungi: A Meta-Analysis , 2017, Front. Microbiol..

[22]  T. Chiou,et al.  Role of vacuoles in phosphorus storage and remobilization. , 2017, Journal of experimental botany.

[23]  Ladislav Nedbal,et al.  Phosphorus from wastewater to crops: An alternative path involving microalgae. , 2016, Biotechnology advances.

[24]  Stephen R Carpenter,et al.  Reducing Phosphorus to Curb Lake Eutrophication is a Success. , 2016, Environmental science & technology.

[25]  J. Elser,et al.  Intensification of phosphorus cycling in China since the 1600s , 2016, Proceedings of the National Academy of Sciences.

[26]  Christopher P. Long,et al.  Heterotrophic bacteria from an extremely phosphate-poor lake have conditionally reduced phosphorus demand and utilize diverse sources of phosphorus. , 2016, Environmental microbiology.

[27]  J. Pittman,et al.  PSR1 Is a Global Transcriptional Regulator of Phosphorus Deficiency Responses and Carbon Storage Metabolism in Chlamydomonas reinhardtii1[OPEN] , 2015, Plant Physiology.

[28]  Stuart White,et al.  Life's Bottleneck: Sustaining the World's Phosphorus for a Food Secure Future , 2014 .

[29]  A. Grossman,et al.  Critical Function of a Chlamydomonas reinhardtii Putative Polyphosphate Polymerase Subunit during Nutrient Deprivation[C][W] , 2014, Plant Cell.

[30]  V. Zachleder,et al.  Effect of nutrient supply status on biomass composition of eukaryotic green microalgae , 2014, Journal of Applied Phycology.

[31]  Benoit Guieysse,et al.  Plant based phosphorus recovery from wastewater via algae and macrophytes. , 2012, Current opinion in biotechnology.

[32]  Elena M. Bennett,et al.  Phosphorus cycle: A broken biogeochemical cycle , 2011, Nature.

[33]  N. Ramankutty,et al.  Agronomic phosphorus imbalances across the world's croplands , 2011, Proceedings of the National Academy of Sciences.

[34]  Natasha Gilbert,et al.  Environment: The disappearing nutrient , 2009, Nature.

[35]  Y. Chisti,et al.  Towards a luxury uptake process via microalgae--defining the polyphosphate dynamics. , 2009, Water research.

[36]  D. Cordell,et al.  The story of phosphorus: Global food security and food for thought , 2009 .

[37]  R. French,et al.  High Sensitivity, Quantitative Measurements of Polyphosphate Using a New DAPI-Based Approach , 2008, Journal of Fluorescence.

[38]  N. Amrhein,et al.  Novel method for the quantification of inorganic polyphosphate (iPoP) in Saccharomyces cerevisiae shows dependence of iPoP content on the growth phase , 2005, Archives of Microbiology.

[39]  A. Grossman,et al.  The LPB1 Gene Is Important for Acclimation of Chlamydomonas reinhardtii to Phosphorus and Sulfur Deprivation1[w] , 2005, Plant Physiology.

[40]  P. Reich,et al.  Global patterns of plant leaf N and P in relation to temperature and latitude. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  V. Rubio,et al.  A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. , 2001, Genes & development.

[42]  A. Grossman,et al.  Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[43]  O. H. Griffith,et al.  A robotics-based automated assay for inorganic and organic phosphates. , 1999, Analytical biochemistry.

[44]  A. Grossman,et al.  High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. , 1998, Genetics.

[45]  A. Grossman,et al.  Biochemical Characterization of the Extracellular Phosphatases Produced by Phosphorus-Deprived Chlamydomonas reinhardtii , 1996, Plant physiology.