Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia.
Microbial hydrolysis of polysaccharides is critical to ecosystem functioning and is of great interest in diverse biotechnological applications, such as biofuel production and bioremediation. Here we demonstrate the use of a new, efficient approach to recover genomes of active polysaccharide degrader...
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oai:doaj.org-article:d5e26c59515147918cf24d87c323c1242021-11-18T07:21:26ZCapturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia.1932-620310.1371/journal.pone.0035314https://doaj.org/article/d5e26c59515147918cf24d87c323c1242012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22536372/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Microbial hydrolysis of polysaccharides is critical to ecosystem functioning and is of great interest in diverse biotechnological applications, such as biofuel production and bioremediation. Here we demonstrate the use of a new, efficient approach to recover genomes of active polysaccharide degraders from natural, complex microbial assemblages, using a combination of fluorescently labeled substrates, fluorescence-activated cell sorting, and single cell genomics. We employed this approach to analyze freshwater and coastal bacterioplankton for degraders of laminarin and xylan, two of the most abundant storage and structural polysaccharides in nature. Our results suggest that a few phylotypes of Verrucomicrobia make a considerable contribution to polysaccharide degradation, although they constituted only a minor fraction of the total microbial community. Genomic sequencing of five cells, representing the most predominant, polysaccharide-active Verrucomicrobia phylotype, revealed significant enrichment in genes encoding a wide spectrum of glycoside hydrolases, sulfatases, peptidases, carbohydrate lyases and esterases, confirming that these organisms were well equipped for the hydrolysis of diverse polysaccharides. Remarkably, this enrichment was on average higher than in the sequenced representatives of Bacteroidetes, which are frequently regarded as highly efficient biopolymer degraders. These findings shed light on the ecological roles of uncultured Verrucomicrobia and suggest specific taxa as promising bioprospecting targets. The employed method offers a powerful tool to rapidly identify and recover discrete genomes of active players in polysaccharide degradation, without the need for cultivation.Manuel Martinez-GarciaDavid M BrazelBrandon K SwanCarol ArnostiPatrick S G ChainKrista G ReitengaGary XieNicole J PoultonMonica Lluesma GomezDashiell E D MaslandBrian ThompsonWendy K BellowsKai ZiervogelChien-Chi LoSanaa AhmedCheryl D GleasnerChris J DetterRamunas StepanauskasPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 4, p e35314 (2012) |
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Medicine R Science Q Manuel Martinez-Garcia David M Brazel Brandon K Swan Carol Arnosti Patrick S G Chain Krista G Reitenga Gary Xie Nicole J Poulton Monica Lluesma Gomez Dashiell E D Masland Brian Thompson Wendy K Bellows Kai Ziervogel Chien-Chi Lo Sanaa Ahmed Cheryl D Gleasner Chris J Detter Ramunas Stepanauskas Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. |
| description |
Microbial hydrolysis of polysaccharides is critical to ecosystem functioning and is of great interest in diverse biotechnological applications, such as biofuel production and bioremediation. Here we demonstrate the use of a new, efficient approach to recover genomes of active polysaccharide degraders from natural, complex microbial assemblages, using a combination of fluorescently labeled substrates, fluorescence-activated cell sorting, and single cell genomics. We employed this approach to analyze freshwater and coastal bacterioplankton for degraders of laminarin and xylan, two of the most abundant storage and structural polysaccharides in nature. Our results suggest that a few phylotypes of Verrucomicrobia make a considerable contribution to polysaccharide degradation, although they constituted only a minor fraction of the total microbial community. Genomic sequencing of five cells, representing the most predominant, polysaccharide-active Verrucomicrobia phylotype, revealed significant enrichment in genes encoding a wide spectrum of glycoside hydrolases, sulfatases, peptidases, carbohydrate lyases and esterases, confirming that these organisms were well equipped for the hydrolysis of diverse polysaccharides. Remarkably, this enrichment was on average higher than in the sequenced representatives of Bacteroidetes, which are frequently regarded as highly efficient biopolymer degraders. These findings shed light on the ecological roles of uncultured Verrucomicrobia and suggest specific taxa as promising bioprospecting targets. The employed method offers a powerful tool to rapidly identify and recover discrete genomes of active players in polysaccharide degradation, without the need for cultivation. |
| format |
article |
| author |
Manuel Martinez-Garcia David M Brazel Brandon K Swan Carol Arnosti Patrick S G Chain Krista G Reitenga Gary Xie Nicole J Poulton Monica Lluesma Gomez Dashiell E D Masland Brian Thompson Wendy K Bellows Kai Ziervogel Chien-Chi Lo Sanaa Ahmed Cheryl D Gleasner Chris J Detter Ramunas Stepanauskas |
| author_facet |
Manuel Martinez-Garcia David M Brazel Brandon K Swan Carol Arnosti Patrick S G Chain Krista G Reitenga Gary Xie Nicole J Poulton Monica Lluesma Gomez Dashiell E D Masland Brian Thompson Wendy K Bellows Kai Ziervogel Chien-Chi Lo Sanaa Ahmed Cheryl D Gleasner Chris J Detter Ramunas Stepanauskas |
| author_sort |
Manuel Martinez-Garcia |
| title |
Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. |
| title_short |
Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. |
| title_full |
Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. |
| title_fullStr |
Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. |
| title_full_unstemmed |
Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. |
| title_sort |
capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of verrucomicrobia. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2012 |
| url |
https://doaj.org/article/d5e26c59515147918cf24d87c323c124 |
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