Sticky or thrifty: Divergence in extracellular glycometabolic architecture underpins contrasting fungal bioflocculation strategies

Jing Zhang; Ruiyi Jin; Liuxu Dong; Chunli Yu; Wei Luo; Yao Hu; Yuqin Zhang; Wei Zhang; Jin Liu; Wenguang Zhou; Shengxi Shao

doi:10.1016/j.watres.2025.124126

Sticky or thrifty: Divergence in extracellular glycometabolic architecture underpins contrasting fungal bioflocculation strategies

Water Res. 2025 Jun 28:285:124126. doi: 10.1016/j.watres.2025.124126. Online ahead of print.

Authors

Jing Zhang¹, Ruiyi Jin¹, Liuxu Dong¹, Chunli Yu¹, Wei Luo¹, Yao Hu¹, Yuqin Zhang¹, Wei Zhang¹, Jin Liu², Wenguang Zhou³, Shengxi Shao⁴

Affiliations

¹ Nanchang University-Imperial College London Joint Laboratory on Photosynthesis and Low Carbon Biotechnology, Key Laboratory of Poyang Lake Environment and Resource Utilization Ministry of Education, School of Resources and Environment, Nanchang University, Nanchang 330031, China.
² Nanchang University-Imperial College London Joint Laboratory on Photosynthesis and Low Carbon Biotechnology, Key Laboratory of Poyang Lake Environment and Resource Utilization Ministry of Education, School of Resources and Environment, Nanchang University, Nanchang 330031, China; Center for Algae Innovation & Engineering Research, Engineering Research Center of Watershed Carbon Neutrality of Ministry of Education, Nanchang University, Nanchang 330031, China.
³ Nanchang University-Imperial College London Joint Laboratory on Photosynthesis and Low Carbon Biotechnology, Key Laboratory of Poyang Lake Environment and Resource Utilization Ministry of Education, School of Resources and Environment, Nanchang University, Nanchang 330031, China; Center for Algae Innovation & Engineering Research, Engineering Research Center of Watershed Carbon Neutrality of Ministry of Education, Nanchang University, Nanchang 330031, China. Electronic address: wgzhou@ncu.edu.cn.
⁴ Nanchang University-Imperial College London Joint Laboratory on Photosynthesis and Low Carbon Biotechnology, Key Laboratory of Poyang Lake Environment and Resource Utilization Ministry of Education, School of Resources and Environment, Nanchang University, Nanchang 330031, China; Center for Algae Innovation & Engineering Research, Engineering Research Center of Watershed Carbon Neutrality of Ministry of Education, Nanchang University, Nanchang 330031, China. Electronic address: s.shao@ncu.edu.cn.

PMID: 40602066
DOI: 10.1016/j.watres.2025.124126

Abstract

Fungal-assisted bioflocculation is attracting attention as a chemical-free route for algal bloom mitigation and pollutants sequestration, but its species-specific traits that govern performance remain poorly quantified, hindering rational strain selection and scale-up. Here, we systematically compared three phylogenetically distinct fungi Aspergillus oryzae, Aspergillus niger and Pleurotus ostreatus interacting with the model cyanobacterium Synechocystis sp. PCC 6803 under bench-scale conditions relevant to drinking-water treatment. Despite producing the highest extracellular polymeric substances (EPS, 213.6 mg/g), Pleurotus ostreatus (Basidiomycota) achieved a 23 % lower harvesting efficiency than Aspergillus oryzae (150.1 mg/g). Quantitative EPS profiling revealed that mannose/galactose-rich glycoproteins in Aspergillus oryzae and ribose-enriched matrices in Aspergillus niger promoted microalgal adhesion, whereas the glucose-dense, storage-oriented EPS of Pleurotus ostreatus limited interfacial activity. Calcium addition further enhanced Aspergillus oryzae removal but impeded Pleurotus ostreatus, indicating clade-specific Ca²⁺-protein bridging mechanisms. Phylogenomic analysis traced these functional divergences to glycometabolic adaptations predating the Ascomycota-Basidiomycota split. We propose a layer-resolved EPS model: Ascomycota evolved surface-active glycan architectures for immediate cell capture, whereas Basidiomycota relies on protein networks that function primarily after surface disruption. This evolutionary-functional framework delivers quantifiable selection criteria, EPS sugar signature, Ca²⁺/protease responsiveness and peripheral thickness, that enable rational fungal selection for scalable and sustainable bioflocculants suitable for modern water-treatment applications.

Keywords: Extracellular polymeric substances; Fungal bioflocculation; Microalgae flocculation efficiency; Phylogenomic modeling; Proteomics.