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Applied and Environmental Microbiology, April 2009, p. 2046-2056, Vol. 75, No. 7
0099-2240/09/$08.00+0     doi:10.1128/AEM.02294-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils ^,

Naomi L. Ward,^1,2, Jean F. Challacombe,^3,4 Peter H. Janssen,^5,6 Bernard Henrissat,⁷ Pedro M. Coutinho,⁷ Martin Wu,^1, Gary Xie,^3,4 Daniel H. Haft,¹ Michelle Sait,^5, Jonathan Badger,¹ Ravi D. Barabote,^3,4 Brent Bradley,¹ Thomas S. Brettin,^3,4 Lauren M. Brinkac,¹ David Bruce,^3,4 Todd Creasy,¹ Sean C. Daugherty,¹ Tanja M. Davidsen,¹ Robert T. DeBoy,¹ J. Chris Detter,^3,4 Robert J. Dodson,¹ A. Scott Durkin,¹ Anuradha Ganapathy,¹ Michelle Gwinn-Giglio,¹ Cliff S. Han,^3,4 Hoda Khouri,¹ Hajnalka Kiss,^3,4 Sagar P. Kothari,¹ Ramana Madupu,¹ Karen E. Nelson,¹ William C. Nelson,¹ Ian Paulsen,¹ Kevin Penn,¹ Qinghu Ren,¹ M. J. Rosovitz,¹ Jeremy D. Selengut,¹ Susmita Shrivastava,¹ Steven A. Sullivan,¹ Roxanne Tapia,^3,4 L. Sue Thompson,^3,4 Kisha L. Watkins,¹ Qi Yang,¹ Chunhui Yu,¹ Nikhat Zafar,¹ Liwei Zhou,¹ and Cheryl R. Kuske^3*

The Institute for Genomic Research, Rockville, Maryland 20850,¹ Center of Marine Biotechnology, Baltimore, Maryland 21202,² Bioscience Division, M888, Los Alamos National Laboratory, Los Alamos, New Mexico 87545,³ Department of Energy Joint Genome Institute, Walnut Creek, California 94598,⁴ Department of Microbiology and Immunology, University of Melbourne, Parkville, Victoria 3010, Australia,⁵ AgResearch Ltd., Palmerston North 4442, New Zealand,⁶ AFMB—Centre National de la Recherche Scientifique, Universités Aix-Marseille I & II, Marseille, France⁷

Received 6 October 2008/ Accepted 22 January 2009

The complete genomes of three strains from the phylum Acidobacteria were compared. Phylogenetic analysis placed them as a unique phylum. They share genomic traits with members of the Proteobacteria, the Cyanobacteria, and the Fungi. The three strains appear to be versatile heterotrophs. Genomic and culture traits indicate the use of carbon sources that span simple sugars to more complex substrates such as hemicellulose, cellulose, and chitin. The genomes encode low-specificity major facilitator superfamily transporters and high-affinity ABC transporters for sugars, suggesting that they are best suited to low-nutrient conditions. They appear capable of nitrate and nitrite reduction but not N₂ fixation or denitrification. The genomes contained numerous genes that encode siderophore receptors, but no evidence of siderophore production was found, suggesting that they may obtain iron via interaction with other microorganisms. The presence of cellulose synthesis genes and a large class of novel high-molecular-weight excreted proteins suggests potential traits for desiccation resistance, biofilm formation, and/or contribution to soil structure. Polyketide synthase and macrolide glycosylation genes suggest the production of novel antimicrobial compounds. Genes that encode a variety of novel proteins were also identified. The abundance of acidobacteria in soils worldwide and the breadth of potential carbon use by the sequenced strains suggest significant and previously unrecognized contributions to the terrestrial carbon cycle. Combining our genomic evidence with available culture traits, we postulate that cells of these isolates are long-lived, divide slowly, exhibit slow metabolic rates under low-nutrient conditions, and are well equipped to tolerate fluctuations in soil hydration.

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* Corresponding author. Mailing address: Bioscience Division, M888, Los Alamos National Laboratory, Los Alamos, NM 87545. Phone: (505) 665-4800. Fax: (505) 665-3024. E-mail: kuske{at}lanl.gov

Published ahead of print on 5 February 2009.

Supplemental material for this article may be found at http://aem.asm.org/.

Present address: Department of Molecular Biology, University of Wyoming, Laramie, WY 82071.

Present address: University of California Davis Genome Center, Davis, CA 95616.

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Applied and Environmental Microbiology, April 2009, p. 2046-2056, Vol. 75, No. 7
0099-2240/09/$08.00+0     doi:10.1128/AEM.02294-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.