TY - JOUR

T1 - A genomic perspective on the potential of Actinobacillus succinogenes for industrial succinate production

AU - McKinlay, James B.

AU - Laivenieks, Maris

AU - Schindler, Bryan D.

AU - McKinlay, Anastasia A.

AU - Siddaramappa, Shivakumara

AU - Challacombe, Jean F.

AU - Lowry, Stephen R.

AU - Clum, Alicia

AU - Lapidus, Alla L.

AU - Burkhart, Kirk B.

AU - Harkins, Victoria

AU - Vieille, Claire

N1 - Funding Information: This work was supported by the National Science Foundation grant BES-0224596, by a grant from the Michigan State University (MSU) Research Excellence Fund, and by a grant from the Michigan Economic Development Corporation. We wish to thank Dr. J. Gregory Zeikus for allowing us to continue his work on this fascinating and useful organism. We are deeply grateful to the JGI for sequencing the A. succinogenes genome and providing us with the automatic annotation and useful genome analysis tools. The U.S. Department of Energy Joint Genome Institute work was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. We also thank Drs. M. Bagdasarian, J.A. Breznak, C.A. Reddy, and Y. Shachar-Hill for valuable insights and discussions. We acknowledge Dr. Carlos Araya for assistance with Python programming. We are grateful to Drs. Peter Bergholz and Hector Alaya-del-Rio for expert advice on manual genome annotations. We thank Christopher B. Jambor for his valuable editing advice.

PY - 2010/11/30

Y1 - 2010/11/30

N2 - Background: Succinate is produced petrochemically from maleic anhydride to satisfy a small specialty chemical market. If succinate could be produced fermentatively at a price competitive with that of maleic anhydride, though, it could replace maleic anhydride as the precursor of many bulk chemicals, transforming a multi-billion dollar petrochemical market into one based on renewable resources. Actinobacillus succinogenes naturally converts sugars and CO2 into high concentrations of succinic acid as part of a mixed-acid fermentation. Efforts are ongoing to maximize carbon flux to succinate to achieve an industrial process.Results: Described here is the 2.3 Mb A. succinogenes genome sequence with emphasis on A. succinogenes's potential for genetic engineering, its metabolic attributes and capabilities, and its lack of pathogenicity. The genome sequence contains 1,690 DNA uptake signal sequence repeats and a nearly complete set of natural competence proteins, suggesting that A. succinogenes is capable of natural transformation. A. succinogenes lacks a complete tricarboxylic acid cycle as well as a glyoxylate pathway, and it appears to be able to transport and degrade about twenty different carbohydrates. The genomes of A. succinogenes and its closest known relative, Mannheimia succiniciproducens, were compared for the presence of known Pasteurellaceae virulence factors. Both species appear to lack the virulence traits of toxin production, sialic acid and choline incorporation into lipopolysaccharide, and utilization of hemoglobin and transferrin as iron sources. Perspectives are also given on the conservation of A. succinogenes genomic features in other sequenced Pasteurellaceae.Conclusions: Both A. succinogenes and M. succiniciproducens genome sequences lack many of the virulence genes used by their pathogenic Pasteurellaceae relatives. The lack of pathogenicity of these two succinogens is an exciting prospect, because comparisons with pathogenic Pasteurellaceae could lead to a better understanding of Pasteurellaceae virulence. The fact that the A. succinogenes genome encodes uptake and degradation pathways for a variety of carbohydrates reflects the variety of carbohydrate substrates available in the rumen, A. succinogenes's natural habitat. It also suggests that many different carbon sources can be used as feedstock for succinate production by A. succinogenes.

AB - Background: Succinate is produced petrochemically from maleic anhydride to satisfy a small specialty chemical market. If succinate could be produced fermentatively at a price competitive with that of maleic anhydride, though, it could replace maleic anhydride as the precursor of many bulk chemicals, transforming a multi-billion dollar petrochemical market into one based on renewable resources. Actinobacillus succinogenes naturally converts sugars and CO2 into high concentrations of succinic acid as part of a mixed-acid fermentation. Efforts are ongoing to maximize carbon flux to succinate to achieve an industrial process.Results: Described here is the 2.3 Mb A. succinogenes genome sequence with emphasis on A. succinogenes's potential for genetic engineering, its metabolic attributes and capabilities, and its lack of pathogenicity. The genome sequence contains 1,690 DNA uptake signal sequence repeats and a nearly complete set of natural competence proteins, suggesting that A. succinogenes is capable of natural transformation. A. succinogenes lacks a complete tricarboxylic acid cycle as well as a glyoxylate pathway, and it appears to be able to transport and degrade about twenty different carbohydrates. The genomes of A. succinogenes and its closest known relative, Mannheimia succiniciproducens, were compared for the presence of known Pasteurellaceae virulence factors. Both species appear to lack the virulence traits of toxin production, sialic acid and choline incorporation into lipopolysaccharide, and utilization of hemoglobin and transferrin as iron sources. Perspectives are also given on the conservation of A. succinogenes genomic features in other sequenced Pasteurellaceae.Conclusions: Both A. succinogenes and M. succiniciproducens genome sequences lack many of the virulence genes used by their pathogenic Pasteurellaceae relatives. The lack of pathogenicity of these two succinogens is an exciting prospect, because comparisons with pathogenic Pasteurellaceae could lead to a better understanding of Pasteurellaceae virulence. The fact that the A. succinogenes genome encodes uptake and degradation pathways for a variety of carbohydrates reflects the variety of carbohydrate substrates available in the rumen, A. succinogenes's natural habitat. It also suggests that many different carbon sources can be used as feedstock for succinate production by A. succinogenes.

UR - http://www.scopus.com/inward/record.url?scp=78649480346&partnerID=8YFLogxK

U2 - 10.1186/1471-2164-11-680

DO - 10.1186/1471-2164-11-680

M3 - Article

C2 - 21118570

AN - SCOPUS:78649480346

VL - 11

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 680

ER -