Journal Article

Diversity and abundance of phosphonate biosynthetic genes in nature

Labeda, David P, Circello, Benjamin, Yu, Xiaomin, Zhang, Jun Kai, Metcalf, William W, Griffin, Benjamin M, Daraghazi, James R, Janga, Sarath C

2013

Overview

Phosphonates, molecules containing direct C-P bonds, comprise a structurally diverse class of natural products with interesting and useful biological properties. Although their synthesis in protozoa was discovered more than fifty years ago, the extent and diversity of phosphonate production in nature remains poorly characterized. The rearrangement of phosphoenolpyruvate (PEP) to phosphonopyruvate, catalyzed by the enzyme PEP mutase (PepM), is shared by the vast majority of known phosphonate biosynthetic pathways. Thus, the pepM gene can be used as a molecular marker to examine the occurrence and abundance of phosphonate-producing organisms. Based on the presence of this gene, phosphonate biosynthesis is common in microbes, with ca. 5% of sequenced genomes and 7% of genome equivalents in metagenomic datasets carrying pepM. Similarly, we detected the pepM gene in ca. 5% of random actinomycete isolates. The pepM-containing gene neighborhoods from twenty-five of these isolates were cloned, sequenced and compared with those found in sequenced genomes. PEP mutase sequence conservation is strongly correlated with conservation of other nearby genes, suggesting that the diversity of phosphonate biosynthetic pathways can be predicted by examining PEP mutase diversity. We used this approach to estimate the range of phosphonate biosynthetic pathways in nature, revealing dozens of discrete groups in pepM amplicons from local soils, while hundreds were observed in metagenomic datasets. Collectively, our analyses show that phosphonate biosynthesis is both common and diverse in nature, suggesting that the role of these molecules in a phosphorus-limited biosphere may be more important than commonly recognized.

• Publisher: NATIONAL ACADEMY OF SCIENCES,National Acad Sciences,National Academy of Sciences
• Subject: Acid soils / Actinobacteria - enzymology / Actinobacteria - genetics / Actinomycetales / Actinomycetes / Bacterial Proteins - genetics / Bacterial Proteins - metabolism / Base Sequence / bioactive properties / biochemical pathways / Biological properties / Biological Sciences / Biomarkers / Biosphere / Biosynthesis / chemical bonding / data collection / Datasets / Enzymes / genes / genetic markers / Genetics / Genomes / Genomics / Libraries / Metagenome / Metagenomics / Microbiota / microorganisms / Molecular biology / Molecular Sequence Data / Molecules / nucleotide sequences / Organophosphonates - metabolism / phosphonates / Phosphonic acids / Phosphotransferases (Phosphomutases) - genetics / Phosphotransferases (Phosphomutases) - metabolism / Protozoa / sequence analysis / soil / Soil Microbiology