Compatible solutes determine the heat resistance of conidia

TY - JOUR

T1 - Compatible solutes determine the heat resistance of conidia

AU - Seekles, Sjoerd J.

AU - van den Brule, Tom

AU - Punt, Maarten

AU - Dijksterhuis, Jan

AU - Arentshorst, Mark

AU - Ijadpanahsaravi, Maryam

AU - Roseboom, Winfried

AU - Meuken, Gwendolin

AU - Ongenae, Véronique

AU - Zwerus, Jordy

AU - Ohm, Robin A.

AU - Kramer, Gertjan

AU - Wösten, Han A.B.

AU - de Winde, Johannes H.

AU - Ram, Arthur F.J.

N1 - Funding Information: The authors wish to thank TIFN for the project management and the expert meetings therein organized and all experts that participated in these meetings. We thank Utrecht Sequencing Facility for providing sequencing service and data. Utrecht Sequencing Facility is subsidized by the University Medical Center Utrecht, Hubrecht Institute, Utrecht University and The Netherlands X-omics Initiative (NWO project 184.034.019). We are grateful to Tim van Leeuwe for his help in the early stages of CRISPR/Cas9 genome editing in the A. niger strains used in this study. We would also like to thank Jaap Visser for his occasional discussion and input in this work. Publisher Copyright: © 2023, The Author(s).

PY - 2023/12

Y1 - 2023/12

N2 - Background: Asexually developed fungal spores (conidia) are key for the massive proliferation and dispersal of filamentous fungi. Germination of conidia and subsequent formation of a mycelium network give rise to many societal problems related to human and animal fungal diseases, post-harvest food spoilage, loss of harvest caused by plant-pathogenic fungi and moulding of buildings. Conidia are highly stress resistant compared to the vegetative mycelium and therefore even more difficult to tackle. Results: In this study, complementary approaches are used to show that accumulation of mannitol and trehalose as the main compatible solutes during spore maturation is a key factor for heat resistance of conidia. Compatible solute concentrations increase during conidia maturation, correlating with increased heat resistance of mature conidia. This maturation only occurs when conidia are attached to the conidiophore. Moreover, conidia of a mutant Aspergillus niger strain, constructed by deleting genes involved in mannitol and trehalose synthesis and consequently containing low concentrations of these compatible solutes, exhibit a sixteen orders of magnitude more sensitive heat shock phenotype compared to wild-type conidia. Cultivation at elevated temperature results in adaptation of conidia with increased heat resistance. Transcriptomic and proteomic analyses revealed two putative heat shock proteins to be upregulated under these conditions. However, conidia of knock-out strains lacking these putative heat shock proteins did not show a reduced heat resistance. Conclusions: Heat stress resistance of fungal conidia is mainly determined by the compatible solute composition established during conidia maturation. To prevent heat resistant fungal spore contaminants, food processing protocols should consider environmental conditions stimulating compatible solute accumulation and potentially use compatible solute biosynthesis as a novel food preservation target.

AB - Background: Asexually developed fungal spores (conidia) are key for the massive proliferation and dispersal of filamentous fungi. Germination of conidia and subsequent formation of a mycelium network give rise to many societal problems related to human and animal fungal diseases, post-harvest food spoilage, loss of harvest caused by plant-pathogenic fungi and moulding of buildings. Conidia are highly stress resistant compared to the vegetative mycelium and therefore even more difficult to tackle. Results: In this study, complementary approaches are used to show that accumulation of mannitol and trehalose as the main compatible solutes during spore maturation is a key factor for heat resistance of conidia. Compatible solute concentrations increase during conidia maturation, correlating with increased heat resistance of mature conidia. This maturation only occurs when conidia are attached to the conidiophore. Moreover, conidia of a mutant Aspergillus niger strain, constructed by deleting genes involved in mannitol and trehalose synthesis and consequently containing low concentrations of these compatible solutes, exhibit a sixteen orders of magnitude more sensitive heat shock phenotype compared to wild-type conidia. Cultivation at elevated temperature results in adaptation of conidia with increased heat resistance. Transcriptomic and proteomic analyses revealed two putative heat shock proteins to be upregulated under these conditions. However, conidia of knock-out strains lacking these putative heat shock proteins did not show a reduced heat resistance. Conclusions: Heat stress resistance of fungal conidia is mainly determined by the compatible solute composition established during conidia maturation. To prevent heat resistant fungal spore contaminants, food processing protocols should consider environmental conditions stimulating compatible solute accumulation and potentially use compatible solute biosynthesis as a novel food preservation target.

KW - Aspergillus niger

KW - Compatible solutes

KW - Food preservation

KW - Fungal spores

KW - Heat shock proteins

KW - Heat stress

KW - Mannitol

KW - Proteomics

KW - Transcriptomics

KW - Trehalose

UR - http://www.scopus.com/inward/record.url?scp=85176287756&partnerID=8YFLogxK

U2 - 10.1186/s40694-023-00168-9

DO - 10.1186/s40694-023-00168-9

M3 - Article

AN - SCOPUS:85176287756

SN - 2054-3085

VL - 10

JO - Fungal Biology and Biotechnology

JF - Fungal Biology and Biotechnology

IS - 1

M1 - 21

ER -