Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass.
Microbial metabolism of plant polysaccharides is an important part of environmental carbon cycling, human nutrition, and industrial processes based on cellulosic bioconversion. Here we demonstrate a broadly applicable method to analyze how microbes catabolize plant polysaccharides that integrates ca...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2014-11-01
|
| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC4230839?pdf=render |
| _version_ | 1818418812145369088 |
|---|---|
| author | Magali Boutard Tristan Cerisy Pierre-Yves Nogue Adriana Alberti Jean Weissenbach Marcel Salanoubat Andrew C Tolonen |
| author_facet | Magali Boutard Tristan Cerisy Pierre-Yves Nogue Adriana Alberti Jean Weissenbach Marcel Salanoubat Andrew C Tolonen |
| author_sort | Magali Boutard |
| collection | DOAJ |
| description | Microbial metabolism of plant polysaccharides is an important part of environmental carbon cycling, human nutrition, and industrial processes based on cellulosic bioconversion. Here we demonstrate a broadly applicable method to analyze how microbes catabolize plant polysaccharides that integrates carbohydrate-active enzyme (CAZyme) assays, RNA sequencing (RNA-seq), and anaerobic growth screening. We apply this method to study how the bacterium Clostridium phytofermentans ferments plant biomass components including glucans, mannans, xylans, galactans, pectins, and arabinans. These polysaccharides are fermented with variable efficiencies, and diauxies prioritize metabolism of preferred substrates. Strand-specific RNA-seq reveals how this bacterium responds to polysaccharides by up-regulating specific groups of CAZymes, transporters, and enzymes to metabolize the constituent sugars. Fifty-six up-regulated CAZymes were purified, and their activities show most polysaccharides are degraded by multiple enzymes, often from the same family, but with divergent rates, specificities, and cellular localizations. CAZymes were then tested in combination to identify synergies between enzymes acting on the same substrate with different catalytic mechanisms. We discuss how these results advance our understanding of how microbes degrade and metabolize plant biomass. |
| first_indexed | 2024-12-14T12:28:37Z |
| format | Article |
| id | doaj.art-5a3d23a6996b4b6d993598fe4af9f068 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-14T12:28:37Z |
| publishDate | 2014-11-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-5a3d23a6996b4b6d993598fe4af9f0682022-12-21T23:01:14ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042014-11-011011e100477310.1371/journal.pgen.1004773Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass.Magali BoutardTristan CerisyPierre-Yves NogueAdriana AlbertiJean WeissenbachMarcel SalanoubatAndrew C TolonenMicrobial metabolism of plant polysaccharides is an important part of environmental carbon cycling, human nutrition, and industrial processes based on cellulosic bioconversion. Here we demonstrate a broadly applicable method to analyze how microbes catabolize plant polysaccharides that integrates carbohydrate-active enzyme (CAZyme) assays, RNA sequencing (RNA-seq), and anaerobic growth screening. We apply this method to study how the bacterium Clostridium phytofermentans ferments plant biomass components including glucans, mannans, xylans, galactans, pectins, and arabinans. These polysaccharides are fermented with variable efficiencies, and diauxies prioritize metabolism of preferred substrates. Strand-specific RNA-seq reveals how this bacterium responds to polysaccharides by up-regulating specific groups of CAZymes, transporters, and enzymes to metabolize the constituent sugars. Fifty-six up-regulated CAZymes were purified, and their activities show most polysaccharides are degraded by multiple enzymes, often from the same family, but with divergent rates, specificities, and cellular localizations. CAZymes were then tested in combination to identify synergies between enzymes acting on the same substrate with different catalytic mechanisms. We discuss how these results advance our understanding of how microbes degrade and metabolize plant biomass.http://europepmc.org/articles/PMC4230839?pdf=render |
| spellingShingle | Magali Boutard Tristan Cerisy Pierre-Yves Nogue Adriana Alberti Jean Weissenbach Marcel Salanoubat Andrew C Tolonen Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. PLoS Genetics |
| title | Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. |
| title_full | Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. |
| title_fullStr | Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. |
| title_full_unstemmed | Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. |
| title_short | Functional diversity of carbohydrate-active enzymes enabling a bacterium to ferment plant biomass. |
| title_sort | functional diversity of carbohydrate active enzymes enabling a bacterium to ferment plant biomass |
| url | http://europepmc.org/articles/PMC4230839?pdf=render |
| work_keys_str_mv | AT magaliboutard functionaldiversityofcarbohydrateactiveenzymesenablingabacteriumtofermentplantbiomass AT tristancerisy functionaldiversityofcarbohydrateactiveenzymesenablingabacteriumtofermentplantbiomass AT pierreyvesnogue functionaldiversityofcarbohydrateactiveenzymesenablingabacteriumtofermentplantbiomass AT adrianaalberti functionaldiversityofcarbohydrateactiveenzymesenablingabacteriumtofermentplantbiomass AT jeanweissenbach functionaldiversityofcarbohydrateactiveenzymesenablingabacteriumtofermentplantbiomass AT marcelsalanoubat functionaldiversityofcarbohydrateactiveenzymesenablingabacteriumtofermentplantbiomass AT andrewctolonen functionaldiversityofcarbohydrateactiveenzymesenablingabacteriumtofermentplantbiomass |