Genomics and Evolution of Symbioses

My lab has done a lot of work on the genomics of symbioses – in particular of bacteria that are found in close associations with plants and animals.  Originally and still some of the time our work has focused on single symbionts at a time, especially those that can be cultured.  Example publications on such specific symbioses (as opposed to studies of whole microbiomes) are given below.

Microbial symbionts of animals.

Chemosynthetic Mutualistic Symbionts

• Newton ILG, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC, Fontanez KM, Lau E, Stewart FJ, Richardson PM, Barry KW, Saunders E, Detter JC, Wu D, Eisen JA, Cavanaugh CM. 2007. The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315: 998-1000. PMID: 17303757.
• Dmytrenko O, Russell SL, Loo WT, Fontanez KM, Liao L, Roeselers G, Sharma R, Stewart FJ, Newton IL, Woyke T, Wu D, Lang JM, Eisen JA, Cavanaugh CM. 2014. The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis. BMC Genomics 15: 924. PMID: 25342549. PMC4287430
• Roeselers G, Newton IL, Woyke T, Auchtung TA, Dilly GF, Dutton RJ, Fisher MC, Fontanez KM, Lau E, Stewart FJ, Richardson PM, Barry KW, Saunders E, Detter JC, Wu D, Eisen JA, Cavanaugh CM. 2010. Complete genome sequence of Candidatus Ruthia magnifica. Standards in Genomic Sciences 3: 163-173.
• Lee RD, Jospin G, Coil DA, Eisen JA. 2014. Draft genome sequence of the endosymbiont “Candidatus Ruthia magnifica” UCD-CM (Phylum Proteobacteria). Genome Announcements 2: e00717-14. PMID: 25035337. PMCID: PMC4102874.
• Eisen JA, Smith SW, Cavanaugh CM. 1992. Phylogenetic relationships of chemoautotrophic bacterial symbionts of Solemya velum Say (Mollusca: Bivalvia) determined by 16S rRNA gene sequence analysis. Journal of Bacteriology 174: 3416-3421. PMID: 1577710. PMCID: PMC206016. PDF.
  
  

Wolbachia Genomics

• Wu M, Sun L, Vamathevan J, Riegler M, Deboy R, Brownlie J, McGraw E, Mohamoud Y, Lee P, Berry K, Khouri HM, Paulsen IT, Nelson KE, Martin W, Esser C, Ahmadinejad N, Wiegand C, Durkin AS, Nelson WC, Beanan MJ, Brinkac LM, Daugherty SC, Dodson RJ, Gwinn M, Kolonay JF, Madupu R, Craven MB, Utterback T, Weidman J, Nierman WC, Aken SV, Tettelin H, O’Neill S, Eisen JA. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome massively infected with mobile genetic elements. PLoS Biology 2: 327-341. PMID: 15024419.
• Pfarr K, Foster J, Slatko B, Hoerauf A, Eisen JA. 2007. On the taxonomic status of the intracellular bacteria Wolbachia pipientis: should this species naming include the intracellular bacteria of filarial nematodes? International Journal of Systematic and Evolutionary Microbiology 57: 1677-1678. PMID: 17684235. PDF.
• Ware J, Moran L, Foster J, Posfai J, Vincze T, Guiliano D, Blaxter M, Eisen JA, Slatko B. 2002. Sequencing and analysis of a 63 kb BAC from the Wolbachia endosymbiont of the human filarial parasite Brugia malayi. International Journal of Parasitology 32: 159-166. PMID: 11812492. PDF.

Other mutualistic symbioses

• Yang JC, Madupu R, Durkin AS, Ekborg NA, Pedamallu CS, Hostetler JB, Radune D, Toms BS, Henrissat B, Coutinho PM, Schwarz S, Field L, Trindade-Silva AE, Soares CA, Elshahawi S, Hanora A, Schmidt EW, Haygood MG, Posfai J, Benner J, Madinger C, Nove J, Anton B, Chaudhary K, Foster J, Holman A, Kumar S, Lessard PA, Luyten YA, Slatko B, Wood N, Wu B, Teplitski M, Mougous JD, Ward N, Eisen JA, Badger JH, Distel DL. 2009. The complete genome of Teredinibacter turnerae T7901: an intracellular endosymbiont of marine wood-boring bivalves (shipworms). PLoS ONE 4: e6085. PMID: 19568419. PDF.
• Campbell BJ, Smith JL, Hanson TE, Klotz MG, Stein LY, Lee CK, Wu D, Robinson JM, Khouri HM, Eisen JA, Cary SC. 2009. Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genetics 5: e1000362. PMID: 19197347. PDF.
• Wu D, Daugherty SC, van Aken S, Pai G, Watkins K, Khouri H, Tallon L, Zaborsky J, Dunbar H, Tran P, Moran NA, Eisen JA. 2006. Metabolic complementarity and genomics of the dual symbiosis of sharpshooters. PLoS Biology 4: e188. PMID: 16729848.
• Schmidt EW, Nelson JT, Rakso D, Sudek S, Eisen JA, Haygood MG, Ravel J. 2005. Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the obligate cyanobacterial symbiont of Lissoclinum patella (ascidia). Proceedings of the National Academy of Sciences USA 102: 7315-7320.  PMID: 15883371. PDF.

Pathogen genomics

• Kozyreva VK, Jospin G, Greninger AL, Watt JP, Eisen JA, Chaturvedi V. 2016. Recent outbreaks of shigellosis in California caused by two distinct populations of Shigella sonnei with either increased virulence or fluoroquinolone resistance. mSphere 1(6): e00344-16.
• Eisen JA, MacCallum CJ. 2009. Genomics of emerging infectious disease: A PLoS collection. PLoS Biology 7: e1000224. PMID: 19855830. PDF.
• Dunning Hotopp JC, Lin M, Madupu R, Crabtree J, Angiuoli SV, Eisen JA, Seshadri R, Ren Q, Wu M, Utterback TR, Smith S, Lewis M, Khouri H, Zhang C, Niu H, Lin Q, Ohashi N, Zhi N, Nelson W, Brinkac LM, Dodson RJ, Rosovitz MJ, Sundaram J, Daugherty SC, Davidsen T, Durkin AS, Gwinn M, Haft DH, Selengut JD, Sullivan SA, Zafar N, Zhou L, Benahmed F, Forberger H, Halpin R, Mulligan S, Robinson J, White O, Rikihisa Y, Tettelin H. 2006. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genetics 2: e21. PMID: 16482227. PDF.
• Ghedin E, Bringaud F, Peterson J, Myler P, Berriman M, Ivens A, Andersson B, Bontempi E, Eisen JA, Angiuoli S, Wanless D, Von Arx A, Murphy L, Lennard N, Salzberg SL, Adams MD, White O, Hall N, Stuart K, Fraser CM, El-Sayed NM. 2004. Gene synteny and evolution of genome architecture in trypanosomatids. Molecular and Biochemical Parasitology 134: 183-191. PMID: 15003838. PDF.
• Seshadri R, Myers GS, Tettelin H, Eisen JA, Heidelberg JF, Dodson RJ, Davidsen TM, DeBoy RT, Fouts DE, Haft DH, Selengut J, Ren Q, Brinkac LM, Madupu R, Kolonay J, Durkin SA, Daugherty SC, Shetty J, Shvartsbeyn A, Gebregeorgis E, Geer K, Tsegaye G, Malek J, Ayodeji B, Shatsman S, McLeod MP, Smajs D, Howell JK, Pal S, Amin A, Vashisth P, McNeill TZ, Xiang Q, Sodergren E, Baca E, Weinstock GM, Norris SJ, Fraser CM, Paulsen IT. 2004. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proceedings of the National Academy of Sciences USA 101: 5646-5651. PMID: 15064399. PDF.
• Nelson KE, Fleischmann RD, DeBoy RT, Paulsen IT, Fouts DE, Eisen JA, Daugherty SC, Dodson RJ, Durkin AS, Gwinn M, Haft DH, Kolonay JF, Nelson WC, Mason T, Tallon L, Gray J, Granger D, Tettelin H, Dong H, Galvin JL, Duncan MJ, Dewhirst FE, Fraser CM. 2003. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. Journal of Bacteriology 185: 5591-5601. PMID: 12949112. PDF.
• Alland D, Whittam TS, Murray MB, Cave MD, Hazbon MH, Dix K, Kokoris M, Duesterhoeft A, Eisen JA, Fraser CM, Fleischmann RD. 2003. Modeling bacterial evolution with comparative-genome-based marker systems: application to Mycobacterium tuberculosis evolution and pathogenesis. Journal of Bacteriology 185: 3392-3399. PMID: 12754238. PDF.
• Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, Nelson WC, Ward NL, Tettelin H, Davidsen TM, Beanan MJ, Deboy RT, Daugherty SC, Brinkac LM, Madupu R, Dodson RJ, Khouri HM, Lee KH, Carty HA, Scanlan D, Heinzen RA, Thompson HA, Samuel JE, Fraser CM, Heidelberg JF. 2003. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proceedings of the National Academy of Sciences USA 100: 5455-5460. PMID: 12704232. PDF.
• Paulsen IT, Banerjei L, Myers GS, Nelson KE, Seshadri R, Read TD, Fouts DE, Eisen JA, Gill SR, Heidelberg JF, Tettelin H, Dodson RJ, Umayam L, Brinkac L, Beanan M, Daugherty S, DeBoy RT, Durkin S, Kolonay J, Madupu R, Nelson W, Vamathevan J, Tran B, Upton J, Hansen T, Shetty J, Khouri H, Utterback T, Radune D, Ketchum KA, Dougherty BA, Fraser CM. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299: 2071-2074. PMID: 12663927. PDF.
• Read TD, Peterson SN, Tourasse N, Baillie LW, Paulsen IT, Nelson KE, Tettelin H, Fouts DE, Eisen JA, Gill SR, Holtzapple EK, Okstad OA, Helgason E, Rilstone J, Wu M, Kolonay JF, Beanan MJ, Dodson RJ, Brinkac LM, Gwinn M, DeBoy RT, Madpu R, Daugherty SC, Durkin AS, Haft DH, Nelson WC, Peterson JD, Pop M, Khouri HM, Radune D, Benton JL, Mahamoud Y, Jiang L, Hance IR, Weidman JF, Berry KJ, Plaut RD, Wolf AM, Watkins KL, Nierman WC, Hazen A, Cline R, Redmond C, Thwaite JE, White O, Salzberg SL, Thomason B, Friedlander AM, Koehler TM, Hanna PC, Kolsto AB, Fraser CM. 2003. The complete genome sequence of Bacillus anthracis Ames and comparison to closely-related B. cereus group bacteria. Nature 423: 81-86. PMID: 12721629. PDF.
• Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511. PMID: 12368864. PDF.
• Paulsen IT, Seshadri R, Nelson KE, Eisen JA, Heidelberg JF, Read TD, Dodson RJ, Umayam L, Brinkac LM, Beanan MJ, Daugherty SC, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Nelson WC, Ayodeji B, Kraul M, Shetty J, Malek J, Van Aken SE, Riedmuller S, Tettelin H, Gill SR, White O, Salzberg SL, Hoover DL, Lindler LE, Halling SM, Boyle SM, Fraser CM. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proceedings of the National Academy of Sciences USA 99: 13148-13153. PMID: 12271122. PDF.
• Fleischmann RD, Alland D, Eisen JA, Carpenter L, White O, Peterson J, DeBoy R, Dodson R, Gwinn M, Haft D, Hickey E, Kolonay JF, Nelson WC, Umayam LA, Ermolaeva M, Salzberg SL, Delcher A, Utterback T, Weidman J, Khouri H, Gill J, Mikula A, Bishai W, Jacobs WR Jr, Venter JC, Fraser CM. 2002. Whole-genome comparison of Mycobacterium tuberculosis clinical and laboratory strains. Journal of Bacteriology 184: 5479-5490. PMID: 12218036. PDF.
• Tettelin H, Masignani V, Cieslewicz MJ, Eisen JA, Peterson S, Wessels MR, Paulsen IT, Nelson KE, Margarit I, Read TD, Madoff LC, Wolf AM, Beanan MJ, Brinkac LM, Daugherty SC, DeBoy RT, Durkin AS, Kolonay JF, Madupu R, Lewis MR, Radune D, Fedorova NB, Scanlan D, Khouri H, Mulligan S, Carty HA, Cline RT, Van Aken SE, Gill J, Scarselli M, Mora M, Iacobini ET, Brettoni C, Galli G, Mariani M, Vegni F, Maione D, Rinaudo D, Rappuoli R, Telford JL, Kasper DL, Grandi G, Fraser CM. 2002. Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proceedings of the National Academy of Sciences USA 99: 12391-12396. PMID: 12200547. PDF.
• Tettelin H, Nelson KE, Paulsen I, Eisen JA, Read TD, Peterson S, Heidelberg J, DeBoy RT, Haft DH, Dodson RJ, Durkin S, Gwinn M, Kolonoay JF, Nelson WC, Peterson JD, Umayam LA, White O, Salzberg SL, Lewis MR, Radune D, Holtzapple E, Khouri H, Wolf AM, Utterback TR, Hansen CK, McDonald LA, Feldblyum TV, Angiuoli S, Dickinson T, Hickey EK, Holt IE, Loftus BJ, Yang F, Smith HO, Venter JC, Dougherty BA, Morrison DA, Hollingshead SK, Fraser CM. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498-506. PMID: 11463916. PDF. Supplemental information
• Read TD, Brunham RC, Shen C, Gill SR, Heidelberg JF, White O, Hickey EK, Peterson J, Utterback T, Berry K, Bass S, Linher K, Weidman J, Khouri H, Craven B, Bowman C, Dodson R, Gwinn M, Nelson W, DeBoy R, Kolonay J, McClarty G, Salzberg SL, Eisen JA, Fraser CM. 2000. Genome sequences of Chlamydia trachomatis MoPn and C. pneumoniae AR39. Nucleic Acids Research 28: 1397-1406. PMID: 10684935. PDF.
• Tettelin H, Saunders NJ, Heidelberg J, Jeffries AC, Nelson KE, Eisen JA, Ketchum KA, Hood DW, Peden JF, Dodson RJ, Nelson WC, Gwinn ML, DeBoy R, Peterson JD, Hickey EK, Haft DH, Salzberg SL, White O, Fleischmann RD, Dougherty BA, Mason T, Ciecko A, Parksey DS, Blair E, Cittone H, Clark EB, Cotton MD, Utterback TR, Khouri H, Qin H, Vamathevan J, Gill J, Scarlato V, Masignani V, Pizza M, Grandi G, Sun L, Smith HO, Fraser CM, Moxon ER, Rappuoli R, Venter JC. 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287: 1809-1815. PMID: 10710307. PDF.
• Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Umayam L, Gill SR, Nelson KE, Read TD, Tettelin H, Richardson D, Ermolaeva MD, Vamathevan J, Bass S, Qin H, Dragoi I, Sellers P, McDonald L, Utterback T, Fleishmann RD, Nierman WC, White O, Salzberg SL, Smith HO, Colwell RR, Mekalanos JJ, Venter JC, Fraser CM. 2000. The genome sequence of Vibrio cholerae, the etiologic agent of cholera. Nature 406: 477-483. PMID: 10952301. PDF. Supplemental information.

Microbial Symbionts of plants

• Mousa WK, Shearer C, Limay-Rios V, Ettinger CL, Eisen JA, Raizada MN. 2016. Root-hair endophyte stacking in finger millet creates a physicochemical barrier to trap the fungal pathogen Fusarium graminearum. Nature Microbiology 1: 16167. PMID: 27669453. Posted to BioRXiv.
• Shehata HR, Ettinger CL, Eisen JA and Raizada MN. 2016. Genes required for the anti-fungal activity of a bacterial endophyte isolated from a corn landrace grown continuously by subsistence farmers since 1000 BC. Frontiers in Microbiology 7: 1548. doi: 10.3389/fmicb.2016.01548
• Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Almeida Jr NF, Woo L, Chen Y, Paulsen IT, Eisen JA, Karp PD, Bovee Sr D, Chapman P, Clendenning J, Deatherage G, Gillet W, Grant C, Kutyavin T, Levy R, Li M-J, McClelland R, Palmieri A, Raymond C, Rouse G, Saenphimmachak C, Wu Z, Romero P, Gordon D, Zhang S, Yoo H, Tao Y, Biddle P, Jung M, Krespan W, Perry M, Gordon-Kamm B, Liao L, Kim S, Hendrick C, Zhao Z-Y, Dolan M, Chumley F, Tingey SC, Tomb J-F, Gordon MP, Olson MV, Nester EW. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294: 2317-2323. PMID: 11743193. PDF.