Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases

ABSTRACT Phosphatases, including phytases, play a major role in cell metabolism, phosphorus cycle, biotechnology, and pathogenic processes. Nevertheless, their discovery by functional metagenomics is challenging. Here, soil metagenomic libraries were successfully screened for genes encoding phosphat...

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Autores principales:	Genis Andrés Castillo Villamizar, Heiko Nacke, Marc Boehning, Kristin Herz, Rolf Daniel
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	SNARE-associated domain functional metagenomics phosphatases phytases soil metagenome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/825beb6ba15a4d78bc960b24f56bbfb5
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spelling	oai:doaj.org-article:825beb6ba15a4d78bc960b24f56bbfb52021-11-15T15:55:14ZFunctional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases10.1128/mBio.01966-182150-7511https://doaj.org/article/825beb6ba15a4d78bc960b24f56bbfb52019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01966-18https://doaj.org/toc/2150-7511ABSTRACT Phosphatases, including phytases, play a major role in cell metabolism, phosphorus cycle, biotechnology, and pathogenic processes. Nevertheless, their discovery by functional metagenomics is challenging. Here, soil metagenomic libraries were successfully screened for genes encoding phosphatase activity. In this context, we report the largest number and diversity of phosphatase genes derived from functional metagenome analysis. Two of the detected gene products carry domains which have never been associated with phosphatase activity before. One of these domains, the SNARE-associated domain DedA, harbors a so-far-overlooked motif present in numerous bacterial SNARE-associated proteins. Our analysis revealed a previously unreported phytase activity of the alkaline phosphatase and sulfatase superfamily (cl23718) and of purple acid phosphatases from nonvegetal origin. This suggests that the classical concept comprising four classes of phytases should be modified and indicates high performance of our screening method for retrieving novel types of phosphatases/phytases hidden in metagenomes of complex environments. IMPORTANCE Phosphorus (P) is a key element involved in numerous cellular processes and essential to meet global food demand. Phosphatases play a major role in cell metabolism and contribute to control the release of P from phosphorylated organic compounds, including phytate. Apart from the relationship with pathogenesis and the enormous economic relevance, phosphatases/phytases are also important for reduction of phosphorus pollution. Almost all known functional phosphatases/phytases are derived from cultured individual microorganisms. We demonstrate here for the first time the potential of functional metagenomics to exploit the phosphatase/phytase pools hidden in environmental soil samples. The recovered diversity of phosphatases/phytases comprises new types and proteins exhibiting largely unknown characteristics, demonstrating the potential of the screening method for retrieving novel target enzymes. The insights gained into the unknown diversity of genes involved in the P cycle highlight the power of function-based metagenomic screening strategies to study Earth’s phosphatase pools.Genis Andrés Castillo VillamizarHeiko NackeMarc BoehningKristin HerzRolf DanielAmerican Society for MicrobiologyarticleSNARE-associated domainfunctional metagenomicsphosphatasesphytasessoil metagenomeMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	SNARE-associated domain functional metagenomics phosphatases phytases soil metagenome Microbiology QR1-502
spellingShingle	SNARE-associated domain functional metagenomics phosphatases phytases soil metagenome Microbiology QR1-502 Genis Andrés Castillo Villamizar Heiko Nacke Marc Boehning Kristin Herz Rolf Daniel Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases
description	ABSTRACT Phosphatases, including phytases, play a major role in cell metabolism, phosphorus cycle, biotechnology, and pathogenic processes. Nevertheless, their discovery by functional metagenomics is challenging. Here, soil metagenomic libraries were successfully screened for genes encoding phosphatase activity. In this context, we report the largest number and diversity of phosphatase genes derived from functional metagenome analysis. Two of the detected gene products carry domains which have never been associated with phosphatase activity before. One of these domains, the SNARE-associated domain DedA, harbors a so-far-overlooked motif present in numerous bacterial SNARE-associated proteins. Our analysis revealed a previously unreported phytase activity of the alkaline phosphatase and sulfatase superfamily (cl23718) and of purple acid phosphatases from nonvegetal origin. This suggests that the classical concept comprising four classes of phytases should be modified and indicates high performance of our screening method for retrieving novel types of phosphatases/phytases hidden in metagenomes of complex environments. IMPORTANCE Phosphorus (P) is a key element involved in numerous cellular processes and essential to meet global food demand. Phosphatases play a major role in cell metabolism and contribute to control the release of P from phosphorylated organic compounds, including phytate. Apart from the relationship with pathogenesis and the enormous economic relevance, phosphatases/phytases are also important for reduction of phosphorus pollution. Almost all known functional phosphatases/phytases are derived from cultured individual microorganisms. We demonstrate here for the first time the potential of functional metagenomics to exploit the phosphatase/phytase pools hidden in environmental soil samples. The recovered diversity of phosphatases/phytases comprises new types and proteins exhibiting largely unknown characteristics, demonstrating the potential of the screening method for retrieving novel target enzymes. The insights gained into the unknown diversity of genes involved in the P cycle highlight the power of function-based metagenomic screening strategies to study Earth’s phosphatase pools.
format	article
author	Genis Andrés Castillo Villamizar Heiko Nacke Marc Boehning Kristin Herz Rolf Daniel
author_facet	Genis Andrés Castillo Villamizar Heiko Nacke Marc Boehning Kristin Herz Rolf Daniel
author_sort	Genis Andrés Castillo Villamizar
title	Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases
title_short	Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases
title_full	Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases
title_fullStr	Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases
title_full_unstemmed	Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases
title_sort	functional metagenomics reveals an overlooked diversity and novel features of soil-derived bacterial phosphatases and phytases
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/825beb6ba15a4d78bc960b24f56bbfb5
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Functional Metagenomics Reveals an Overlooked Diversity and Novel Features of Soil-Derived Bacterial Phosphatases and Phytases

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