Hydrophobins from Mediate Fungal Interactions with Microplastics

Overview

Journal bioRxiv

Date 2024 Nov 22

PMID 39574658

Authors

Ross R Klauer

Rachel Silvestri

Hanna White

Richard D Hayes

Robert Riley

Anna Lipzen

Kerrie Barry

Igor V Grigoriev

Jayson Talag

Victoria Bunting

Zachary Stevenson

Kevin V Solomon

Mark Blenner

Affiliations

Soon will be listed here.

Abstract

Microplastics present myriad ecological and human health risks including serving as a vector for pathogens in human and animal food chains. However, the specific mechanisms by which pathogenic fungi colonize these microplastics have yet to be explored. In this work, we examine the opportunistic fungal pathogen, and other common soil and marine , which we found bind microplastics tightly. Up to 3.85+/- 1.48 g microplastic plastic/g fungi were bound and flocculated for polypropylene (PP), polyethylene (PE), and polyethylene terephthalate (PET) powders and particles ranging in size from 0.05 - 5 mm. Gene knockouts revealed hydrophobins as a key biomolecule driving microplastic-fungi binding. Moreover, purified hydrophobins were still able to flocculate microplastics independent of the fungus. Our work elucidates a role for hydrophobins in fungal colonization of microplastics and highlights a potential target for mitigating the harm of microplastics through engineered fungal-microplastic interactions.

References

Kettner M, Rojas-Jimenez K, Oberbeckmann S, Labrenz M, Grossart H . Microplastics alter composition of fungal communities in aquatic ecosystems. Environ Microbiol. 2017; 19(11):4447-4459. DOI: 10.1111/1462-2920.13891. View

Schwartz C, Shabbir-Hussain M, Frogue K, Blenner M, Wheeldon I . Standardized Markerless Gene Integration for Pathway Engineering in Yarrowia lipolytica. ACS Synth Biol. 2016; 6(3):402-409. DOI: 10.1021/acssynbio.6b00285. View

Kusuya Y, Takahashi-Nakaguchi A, Takahashi H, Yaguchi T . Draft Genome Sequence of the Pathogenic Filamentous Fungus Aspergillus udagawae Strain IFM 46973T. Genome Announc. 2015; 3(4). PMC: 4541281. DOI: 10.1128/genomeA.00834-15. View

Wu X, Pan J, Li M, Li Y, Bartlam M, Wang Y . Selective enrichment of bacterial pathogens by microplastic biofilm. Water Res. 2019; 165:114979. DOI: 10.1016/j.watres.2019.114979. View

Skerker J, Pianalto K, Mondo S, Yang K, Arkin A, Keller N . Chromosome assembled and annotated genome sequence of Aspergillus flavus NRRL 3357. G3 (Bethesda). 2021; 11(8). PMC: 8496237. DOI: 10.1093/g3journal/jkab213. View

OToole G, Kaplan H, Kolter R . Biofilm formation as microbial development. Annu Rev Microbiol. 2000; 54:49-79. DOI: 10.1146/annurev.micro.54.1.49. View

Wright S, Kelly F . Plastic and Human Health: A Micro Issue?. Environ Sci Technol. 2017; 51(12):6634-6647. DOI: 10.1021/acs.est.7b00423. View

Yang Y, Liu W, Zhang Z, Grossart H, Gadd G . Microplastics provide new microbial niches in aquatic environments. Appl Microbiol Biotechnol. 2020; 104(15):6501-6511. PMC: 7347703. DOI: 10.1007/s00253-020-10704-x. View

Hu C, Garcia M, Nihart A, Liu R, Yin L, Adolphi N . Microplastic presence in dog and human testis and its potential association with sperm count and weights of testis and epididymis. Toxicol Sci. 2024; 200(2):235-240. PMC: 11285152. DOI: 10.1093/toxsci/kfae060. View

10.

Ma H, Pu S, Liu S, Bai Y, Mandal S, Xing B . Microplastics in aquatic environments: Toxicity to trigger ecological consequences. Environ Pollut. 2020; 261:114089. DOI: 10.1016/j.envpol.2020.114089. View

11.

Ragusa A, Svelato A, Santacroce C, Catalano P, Notarstefano V, Carnevali O . Plasticenta: First evidence of microplastics in human placenta. Environ Int. 2021; 146:106274. DOI: 10.1016/j.envint.2020.106274. View

12.

Takahashi T, Maeda H, Yoneda S, Ohtaki S, Yamagata Y, Hasegawa F . The fungal hydrophobin RolA recruits polyesterase and laterally moves on hydrophobic surfaces. Mol Microbiol. 2005; 57(6):1780-96. DOI: 10.1111/j.1365-2958.2005.04803.x. View

13.

Kjaerbolling I, Vesth T, Frisvad J, Nybo J, Theobald S, Kuo A . Linking secondary metabolites to gene clusters through genome sequencing of six diverse species. Proc Natl Acad Sci U S A. 2018; 115(4):E753-E761. PMC: 5789934. DOI: 10.1073/pnas.1715954115. View

14.

Revell L . phytools 2.0: an updated R ecosystem for phylogenetic comparative methods (and other things). PeerJ. 2024; 12:e16505. PMC: 10773453. DOI: 10.7717/peerj.16505. View

15.

Tanaka T, Nakayama M, Takahashi T, Nanatani K, Yamagata Y, Abe K . Analysis of the ionic interaction between the hydrophobin RodA and two cutinases of Aspergillus nidulans obtained via an Aspergillus oryzae expression system. Appl Microbiol Biotechnol. 2016; 101(6):2343-2356. DOI: 10.1007/s00253-016-7979-5. View

16.

Luo H, Liu C, He D, Xu J, Sun J, Li J . Environmental behaviors of microplastics in aquatic systems: A systematic review on degradation, adsorption, toxicity and biofilm under aging conditions. J Hazard Mater. 2021; 423(Pt A):126915. DOI: 10.1016/j.jhazmat.2021.126915. View

17.

Sunde M, Kwan A, Templeton M, Beever R, Mackay J . Structural analysis of hydrophobins. Micron. 2007; 39(7):773-84. DOI: 10.1016/j.micron.2007.08.003. View

18.

Puspitasari N, Tsai S, Lee C . Fungal Hydrophobin RolA Enhanced PETase Hydrolysis of Polyethylene Terephthalate. Appl Biochem Biotechnol. 2020; 193(5):1284-1295. DOI: 10.1007/s12010-020-03358-y. View

19.

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View

20.

Khalid N, Aqeel M, Noman A, Hashem M, Mostafa Y, Alhaithloul H . Linking effects of microplastics to ecological impacts in marine environments. Chemosphere. 2020; 264(Pt 2):128541. DOI: 10.1016/j.chemosphere.2020.128541. View