Frequent Acquisition of Glycoside Hydrolase Family 32 (GH32) Genes from Bacteria via Horizontal Gene Transfer Drives Adaptation of Invertebrates to Diverse Sources of Food and Living Habitats

Cheng, Xiaoyan; Liu, Xuming; Jordan, Katherine W.; Yu, Jingcheng; Whitworth, Robert J.; Park, Yoonseong; Chen, Ming-Shun

doi:10.3390/ijms25158296

Open AccessArticle

Frequent Acquisition of Glycoside Hydrolase Family 32 (GH32) Genes from Bacteria via Horizontal Gene Transfer Drives Adaptation of Invertebrates to Diverse Sources of Food and Living Habitats

by

Xiaoyan Cheng

¹,

Xuming Liu

^1,2,

Katherine W. Jordan

²

,

Jingcheng Yu

³,

Robert J. Whitworth

¹,

Yoonseong Park

¹

and

Ming-Shun Chen

^1,2,*

¹

Department of Entomology, 123 Waters Hall, Kansas State University, Manhattan, KS 66506, USA

²

Hard Winter Wheat Genetics Research Unit, Center for Grain and Animal Health Research, US Department of Agriculture, Agricultural Research Services, 4008 Throckmorton Hall, Kansas State University, Manhattan, KS 66506, USA

³

Department of Biochemistry and Molecular Biophysics, 141 Chalmers Hall, Kansas State University, Manhattan, KS 66506, USA

^*

Author to whom correspondence should be addressed.

Int. J. Mol. Sci. 2024, 25(15), 8296; https://doi.org/10.3390/ijms25158296

Submission received: 19 June 2024 / Revised: 23 July 2024 / Accepted: 24 July 2024 / Published: 30 July 2024

(This article belongs to the Section Biochemistry)

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Abstract

Glycoside hydrolases (GHs, also called glycosidases) catalyze the hydrolysis of glycosidic bonds in polysaccharides. Numerous GH genes have been identified from various organisms and are classified into 188 families, abbreviated GH1 to GH188. Enzymes in the GH32 family hydrolyze fructans, which are present in approximately 15% of flowering plants and are widespread across microorganisms. GH32 genes are rarely found in animals, as fructans are not a typical carbohydrate source utilized in animals. Here, we report the discovery of 242 GH32 genes identified in 84 animal species, ranging from nematodes to crabs. Genetic analyses of these genes indicated that the GH32 genes in various animals were derived from different bacteria via multiple, independent horizontal gene transfer events. The GH32 genes in animals appear functional based on the highly conserved catalytic blades and triads in the active center despite the overall low (35–60%) sequence similarities among the predicted proteins. The acquisition of GH32 genes by animals may have a profound impact on sugar metabolism for the recipient organisms. Our results together with previous reports suggest that the acquired GH32 enzymes may not only serve as digestive enzymes, but also may serve as effectors for manipulating host plants, and as metabolic enzymes in the non-digestive tissues of certain animals. Our results provide a foundation for future studies on the significance of horizontally transferred GH32 genes in animals. The information reported here enriches our knowledge of horizontal gene transfer, GH32 functions, and animal–plant interactions, which may result in practical applications. For example, developing crops via targeted engineering that inhibits GH32 enzymes could aid in the plant’s resistance to animal pests.

Keywords: GH32; glycoside hydrolase family 32; horizontal gene transfer; sugar metabolism

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MDPI and ACS Style

Cheng, X.; Liu, X.; Jordan, K.W.; Yu, J.; Whitworth, R.J.; Park, Y.; Chen, M.-S. Frequent Acquisition of Glycoside Hydrolase Family 32 (GH32) Genes from Bacteria via Horizontal Gene Transfer Drives Adaptation of Invertebrates to Diverse Sources of Food and Living Habitats. Int. J. Mol. Sci. 2024, 25, 8296. https://doi.org/10.3390/ijms25158296

AMA Style

Cheng X, Liu X, Jordan KW, Yu J, Whitworth RJ, Park Y, Chen M-S. Frequent Acquisition of Glycoside Hydrolase Family 32 (GH32) Genes from Bacteria via Horizontal Gene Transfer Drives Adaptation of Invertebrates to Diverse Sources of Food and Living Habitats. International Journal of Molecular Sciences. 2024; 25(15):8296. https://doi.org/10.3390/ijms25158296

Chicago/Turabian Style

Cheng, Xiaoyan, Xuming Liu, Katherine W. Jordan, Jingcheng Yu, Robert J. Whitworth, Yoonseong Park, and Ming-Shun Chen. 2024. "Frequent Acquisition of Glycoside Hydrolase Family 32 (GH32) Genes from Bacteria via Horizontal Gene Transfer Drives Adaptation of Invertebrates to Diverse Sources of Food and Living Habitats" International Journal of Molecular Sciences 25, no. 15: 8296. https://doi.org/10.3390/ijms25158296

APA Style

Cheng, X., Liu, X., Jordan, K. W., Yu, J., Whitworth, R. J., Park, Y., & Chen, M.-S. (2024). Frequent Acquisition of Glycoside Hydrolase Family 32 (GH32) Genes from Bacteria via Horizontal Gene Transfer Drives Adaptation of Invertebrates to Diverse Sources of Food and Living Habitats. International Journal of Molecular Sciences, 25(15), 8296. https://doi.org/10.3390/ijms25158296

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Frequent Acquisition of Glycoside Hydrolase Family 32 (GH32) Genes from Bacteria via Horizontal Gene Transfer Drives Adaptation of Invertebrates to Diverse Sources of Food and Living Habitats

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