Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia

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Title: Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia
Authors: Martinez-Garcia, Manuel | Brazel, David M. | Swan, Brandon K. | Arnosti, Carol | Chain, Patrick S.G. | Reitenga, Krista G. | Xie, Gary | Poulton, Nicole J. | Lluesma Gómez, Mónica | Masland, Dashiell E.D. | Thompson, Brian | Bellows, Wendy K. | Ziervogel, Kai | Lo, Chien-Chi | Ahmed, Sanaa | Gleasner, Cheryl D. | Detter, Chris J. | Stepanauskas, Ramunas
Research Group/s: Ecología Microbiana Molecular
Center, Department or Service: Universidad de Alicante. Departamento de Fisiología, Genética y Microbiología
Keywords: Microbial hydrolysis | Single cell genomes | Polysaccharide degraders | Verrucomicrobia
Knowledge Area: Microbiología
Issue Date: 20-Apr-2012
Publisher: Public Library of Science (PLoS)
Citation: Martinez-Garcia M, Brazel DM, Swan BK, Arnosti C, Chain PSG, et al. (2012) Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia. PLoS ONE 7(4): e35314. doi:10.1371/journal.pone.0035314
Abstract: 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.
Sponsor: This research was supported by the NSF grants DEB-841933 and OCE-821374 to RS, OCE-0848703 to CA and by a Maine Technology Institute research infrastructure grant to the Bigelow Laboratory. The Los Alamos National Laboratory researchers were supported in part by the U.S. Department of Energy Joint Genome Institute through the Office of Science of the U.S. Department of Energy under Contract Number DE-AC02-05CH11231 and grants from the U.S. Defense Threat Reduction Agency under contract numbers B104153I and B084531I.
ISSN: 1932-6203
DOI: 10.1371/journal.pone.0035314
Language: eng
Type: info:eu-repo/semantics/article
Rights: This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Peer Review: si
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