Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria

ABSTRACT Zinc is an essential nutrient in biological systems due to its structural or catalytic requirement in proteins involved in diverse cellular processes. To meet this cellular demand, microbes must acquire sufficient zinc from their environment. However, many environments have low zinc availab...

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Autores principales:	Jacqueline R. Morey, Thomas E. Kehl-Fie
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	metallophore metalloproteins staphylopine zinc Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dfbcdfda8e914373866d73ef111e06fa
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spelling	oai:doaj.org-article:dfbcdfda8e914373866d73ef111e06fa2021-12-02T19:47:35ZBioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria10.1128/mSystems.00554-202379-5077https://doaj.org/article/dfbcdfda8e914373866d73ef111e06fa2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00554-20https://doaj.org/toc/2379-5077ABSTRACT Zinc is an essential nutrient in biological systems due to its structural or catalytic requirement in proteins involved in diverse cellular processes. To meet this cellular demand, microbes must acquire sufficient zinc from their environment. However, many environments have low zinc availability. One of the mechanisms used by bacteria to acquire zinc is through the production of small molecules known as zincophores. Similar to bacterial siderophores used for iron uptake, zincophores are synthesized by the bacterium and exported and then reimported as zincophore-zinc complexes. Thus far, only four zincophores have been described, including two from the human pathogens Staphylococcus aureus and Pseudomonas aeruginosa, in which they play a critical role in zinc acquisition during infection, and one in a soil bacterium. To determine what other microbes may produce zincophores, we used bioinformatic analyses to identify new zincophore biosynthetic gene clusters (BGCs) and predict the diversity of molecules synthesized. Genome neighborhood network analysis identified approximately 250 unique zincophore-producing species from actinobacteria, firmicutes, proteobacteria, and fusobacteria. This indicates that zincophores are produced by diverse bacteria that inhabit a broad range of ecological niches. Many of the BGCs likely produce characterized zincophores, based on similarity to the characterized systems. However, this analysis also identified numerous BGCs that, based on the colocalization of additional modifying enzymes and sequence divergence of the biosynthetic enzymes, are likely to produce unique zincophores. Collectively, these findings provide a comprehensive understanding of the zincophore biosynthetic landscape that will be invaluable for future research on these important small molecules. IMPORTANCE Bacteria must acquire essential nutrients, including zinc, from their environment. For bacterial pathogens, this necessitates overcoming the host metal-withholding response known as nutritional immunity. A novel type of zinc uptake mechanism that involves the bacterial production of a small zinc-scavenging molecule was recently described in the human pathogens Staphylococcus aureus, Pseudomonas aeruginosa, and Yersinia pestis, as well as the soil-associated bacterium Paenibacillus mucilaginosus. This suggests that zincophores may be important for zinc acquisition in diverse environments. In this study, we sought to identify other zincophore-producing bacteria using bioinformatics. We identified almost 250 unique zincophore-producing species, including human and animal pathogens, as well as isolates from soil, rhizosphere, plant, and marine habitats. Crucially, we observed diversity at the amino acid and gene organization levels, suggesting that many of these species are producing unique zincophores. Together, our findings highlight the importance of zincophores for a broad array of bacteria living in diverse environments.Jacqueline R. MoreyThomas E. Kehl-FieAmerican Society for MicrobiologyarticlemetallophoremetalloproteinsstaphylopinezincMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	metallophore metalloproteins staphylopine zinc Microbiology QR1-502
spellingShingle	metallophore metalloproteins staphylopine zinc Microbiology QR1-502 Jacqueline R. Morey Thomas E. Kehl-Fie Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria
description	ABSTRACT Zinc is an essential nutrient in biological systems due to its structural or catalytic requirement in proteins involved in diverse cellular processes. To meet this cellular demand, microbes must acquire sufficient zinc from their environment. However, many environments have low zinc availability. One of the mechanisms used by bacteria to acquire zinc is through the production of small molecules known as zincophores. Similar to bacterial siderophores used for iron uptake, zincophores are synthesized by the bacterium and exported and then reimported as zincophore-zinc complexes. Thus far, only four zincophores have been described, including two from the human pathogens Staphylococcus aureus and Pseudomonas aeruginosa, in which they play a critical role in zinc acquisition during infection, and one in a soil bacterium. To determine what other microbes may produce zincophores, we used bioinformatic analyses to identify new zincophore biosynthetic gene clusters (BGCs) and predict the diversity of molecules synthesized. Genome neighborhood network analysis identified approximately 250 unique zincophore-producing species from actinobacteria, firmicutes, proteobacteria, and fusobacteria. This indicates that zincophores are produced by diverse bacteria that inhabit a broad range of ecological niches. Many of the BGCs likely produce characterized zincophores, based on similarity to the characterized systems. However, this analysis also identified numerous BGCs that, based on the colocalization of additional modifying enzymes and sequence divergence of the biosynthetic enzymes, are likely to produce unique zincophores. Collectively, these findings provide a comprehensive understanding of the zincophore biosynthetic landscape that will be invaluable for future research on these important small molecules. IMPORTANCE Bacteria must acquire essential nutrients, including zinc, from their environment. For bacterial pathogens, this necessitates overcoming the host metal-withholding response known as nutritional immunity. A novel type of zinc uptake mechanism that involves the bacterial production of a small zinc-scavenging molecule was recently described in the human pathogens Staphylococcus aureus, Pseudomonas aeruginosa, and Yersinia pestis, as well as the soil-associated bacterium Paenibacillus mucilaginosus. This suggests that zincophores may be important for zinc acquisition in diverse environments. In this study, we sought to identify other zincophore-producing bacteria using bioinformatics. We identified almost 250 unique zincophore-producing species, including human and animal pathogens, as well as isolates from soil, rhizosphere, plant, and marine habitats. Crucially, we observed diversity at the amino acid and gene organization levels, suggesting that many of these species are producing unique zincophores. Together, our findings highlight the importance of zincophores for a broad array of bacteria living in diverse environments.
format	article
author	Jacqueline R. Morey Thomas E. Kehl-Fie
author_facet	Jacqueline R. Morey Thomas E. Kehl-Fie
author_sort	Jacqueline R. Morey
title	Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria
title_short	Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria
title_full	Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria
title_fullStr	Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria
title_full_unstemmed	Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria
title_sort	bioinformatic mapping of opine-like zincophore biosynthesis in bacteria
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/dfbcdfda8e914373866d73ef111e06fa
work_keys_str_mv	AT jacquelinermorey bioinformaticmappingofopinelikezincophorebiosynthesisinbacteria AT thomasekehlfie bioinformaticmappingofopinelikezincophorebiosynthesisinbacteria
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Bioinformatic Mapping of Opine-Like Zincophore Biosynthesis in Bacteria

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