Discovery of enzymes for toluene synthesis from anoxic microbial communities

Harry R. Beller, Andria V. Rodrigues, Kamrun Zargar, Yu Wei Wu, Avneesh K. Saini, Renee M. Saville, Jose H. Pereira, Paul D. Adams, Susannah G. Tringe, Christopher J. Petzold, Jay D. Keasling

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

Microbial toluene biosynthesis was reported in anoxic lake sediments more than three decades ago, but the enzyme catalyzing this biochemically challenging reaction has never been identified. Here we report the toluene-producing enzyme PhdB, a glycyl radical enzyme of bacterial origin that catalyzes phenylacetate decarboxylation, and its cognate activating enzyme PhdA, a radical S-adenosylmethionine enzyme, discovered in two distinct anoxic microbial communities that produce toluene. The unconventional process of enzyme discovery from a complex microbial community (>300,000 genes), rather than from a microbial isolate, involved metagenomics- and metaproteomics-enabled biochemistry, as well as in vitro confirmation of activity with recombinant enzymes. This work expands the known catalytic range of glycyl radical enzymes (only seven reaction types had been characterized previously) and aromatic-hydrocarbon-producing enzymes, and will enable first-time biochemical synthesis of an aromatic fuel hydrocarbon from renewable resources, such as lignocellulosic biomass, rather than from petroleum.

Original languageEnglish
Pages (from-to)451-457
Number of pages7
JournalNature Chemical Biology
Volume14
Issue number5
DOIs
Publication statusPublished - May 1 2018

Fingerprint

Toluene
Enzymes
Aromatic Hydrocarbons
Metagenomics
S-Adenosylmethionine
Decarboxylation
Petroleum
Lakes
Biochemistry
Biomass

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

Beller, H. R., Rodrigues, A. V., Zargar, K., Wu, Y. W., Saini, A. K., Saville, R. M., ... Keasling, J. D. (2018). Discovery of enzymes for toluene synthesis from anoxic microbial communities. Nature Chemical Biology, 14(5), 451-457. https://doi.org/10.1038/s41589-018-0017-4

Discovery of enzymes for toluene synthesis from anoxic microbial communities. / Beller, Harry R.; Rodrigues, Andria V.; Zargar, Kamrun; Wu, Yu Wei; Saini, Avneesh K.; Saville, Renee M.; Pereira, Jose H.; Adams, Paul D.; Tringe, Susannah G.; Petzold, Christopher J.; Keasling, Jay D.

In: Nature Chemical Biology, Vol. 14, No. 5, 01.05.2018, p. 451-457.

Research output: Contribution to journalArticle

Beller, HR, Rodrigues, AV, Zargar, K, Wu, YW, Saini, AK, Saville, RM, Pereira, JH, Adams, PD, Tringe, SG, Petzold, CJ & Keasling, JD 2018, 'Discovery of enzymes for toluene synthesis from anoxic microbial communities', Nature Chemical Biology, vol. 14, no. 5, pp. 451-457. https://doi.org/10.1038/s41589-018-0017-4
Beller, Harry R. ; Rodrigues, Andria V. ; Zargar, Kamrun ; Wu, Yu Wei ; Saini, Avneesh K. ; Saville, Renee M. ; Pereira, Jose H. ; Adams, Paul D. ; Tringe, Susannah G. ; Petzold, Christopher J. ; Keasling, Jay D. / Discovery of enzymes for toluene synthesis from anoxic microbial communities. In: Nature Chemical Biology. 2018 ; Vol. 14, No. 5. pp. 451-457.
@article{9c3d56d754e7498f84092692d2f5e07d,
title = "Discovery of enzymes for toluene synthesis from anoxic microbial communities",
abstract = "Microbial toluene biosynthesis was reported in anoxic lake sediments more than three decades ago, but the enzyme catalyzing this biochemically challenging reaction has never been identified. Here we report the toluene-producing enzyme PhdB, a glycyl radical enzyme of bacterial origin that catalyzes phenylacetate decarboxylation, and its cognate activating enzyme PhdA, a radical S-adenosylmethionine enzyme, discovered in two distinct anoxic microbial communities that produce toluene. The unconventional process of enzyme discovery from a complex microbial community (>300,000 genes), rather than from a microbial isolate, involved metagenomics- and metaproteomics-enabled biochemistry, as well as in vitro confirmation of activity with recombinant enzymes. This work expands the known catalytic range of glycyl radical enzymes (only seven reaction types had been characterized previously) and aromatic-hydrocarbon-producing enzymes, and will enable first-time biochemical synthesis of an aromatic fuel hydrocarbon from renewable resources, such as lignocellulosic biomass, rather than from petroleum.",
author = "Beller, {Harry R.} and Rodrigues, {Andria V.} and Kamrun Zargar and Wu, {Yu Wei} and Saini, {Avneesh K.} and Saville, {Renee M.} and Pereira, {Jose H.} and Adams, {Paul D.} and Tringe, {Susannah G.} and Petzold, {Christopher J.} and Keasling, {Jay D.}",
year = "2018",
month = "5",
day = "1",
doi = "10.1038/s41589-018-0017-4",
language = "English",
volume = "14",
pages = "451--457",
journal = "Nature Chemical Biology",
issn = "1552-4450",
publisher = "Nature Publishing Group",
number = "5",

}

TY - JOUR

T1 - Discovery of enzymes for toluene synthesis from anoxic microbial communities

AU - Beller, Harry R.

AU - Rodrigues, Andria V.

AU - Zargar, Kamrun

AU - Wu, Yu Wei

AU - Saini, Avneesh K.

AU - Saville, Renee M.

AU - Pereira, Jose H.

AU - Adams, Paul D.

AU - Tringe, Susannah G.

AU - Petzold, Christopher J.

AU - Keasling, Jay D.

PY - 2018/5/1

Y1 - 2018/5/1

N2 - Microbial toluene biosynthesis was reported in anoxic lake sediments more than three decades ago, but the enzyme catalyzing this biochemically challenging reaction has never been identified. Here we report the toluene-producing enzyme PhdB, a glycyl radical enzyme of bacterial origin that catalyzes phenylacetate decarboxylation, and its cognate activating enzyme PhdA, a radical S-adenosylmethionine enzyme, discovered in two distinct anoxic microbial communities that produce toluene. The unconventional process of enzyme discovery from a complex microbial community (>300,000 genes), rather than from a microbial isolate, involved metagenomics- and metaproteomics-enabled biochemistry, as well as in vitro confirmation of activity with recombinant enzymes. This work expands the known catalytic range of glycyl radical enzymes (only seven reaction types had been characterized previously) and aromatic-hydrocarbon-producing enzymes, and will enable first-time biochemical synthesis of an aromatic fuel hydrocarbon from renewable resources, such as lignocellulosic biomass, rather than from petroleum.

AB - Microbial toluene biosynthesis was reported in anoxic lake sediments more than three decades ago, but the enzyme catalyzing this biochemically challenging reaction has never been identified. Here we report the toluene-producing enzyme PhdB, a glycyl radical enzyme of bacterial origin that catalyzes phenylacetate decarboxylation, and its cognate activating enzyme PhdA, a radical S-adenosylmethionine enzyme, discovered in two distinct anoxic microbial communities that produce toluene. The unconventional process of enzyme discovery from a complex microbial community (>300,000 genes), rather than from a microbial isolate, involved metagenomics- and metaproteomics-enabled biochemistry, as well as in vitro confirmation of activity with recombinant enzymes. This work expands the known catalytic range of glycyl radical enzymes (only seven reaction types had been characterized previously) and aromatic-hydrocarbon-producing enzymes, and will enable first-time biochemical synthesis of an aromatic fuel hydrocarbon from renewable resources, such as lignocellulosic biomass, rather than from petroleum.

UR - http://www.scopus.com/inward/record.url?scp=85044178994&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85044178994&partnerID=8YFLogxK

U2 - 10.1038/s41589-018-0017-4

DO - 10.1038/s41589-018-0017-4

M3 - Article

VL - 14

SP - 451

EP - 457

JO - Nature Chemical Biology

JF - Nature Chemical Biology

SN - 1552-4450

IS - 5

ER -