Metabolic reprogramming by viruses in the sunlit and dark ocean

Genome Biology

Volumn 14, Issue 11, 2013, Pages

  Hurwitz, Bonnie L ^a   Hallam, Steven J ^b   Sullivan, Matthew B ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CELL DNA; RIBOSOME RNA; ACETYL COENZYME A; ACETYL COENZYME A CARBOXYLASE; EPIMERASE; FUMARATE HYDRATASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HYDRACRYLIC ACID; ISOCITRATE LYASE; LONG CHAIN FATTY ACID; MANNOSE PHOSPHATE ISOMERASE; METHYLMALONYL COENZYME A MUTASE; PHOSPHOGLUCONATE DEHYDROGENASE; PROPIONYL COENZYME A CARBOXYLASE; PYRUVATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RIBOSEPHOSPHATE PYROPHOSPHOKINASE; RNA 16S; SMALL SUBUNIT RIBOSOMAL RNA; TRANSALDOLASE; TRANSKETOLASE; VIRUS RNA;

ARTICLE; CARBON METABOLISM; CONTROLLED STUDY; ENERGY YIELD; MARINE SPECIES; METABOLIC REGULATION; METABOLISM; MICROBIAL COMMUNITY; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT; PACIFIC OCEAN; SUNLIGHT; TAXONOMY; VIRUS; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION; ACC GENE; AEROMONAS; ALCANIVORAX; ALPHAPROTEOBACTERIA; AMINO ACID METABOLISM; BACTERIUM CONTAMINATION; CARBON FIXATION; CHEMOTROPH; CONTIG MAPPING; CYANOPHAGE; DARK OCEAN; ENERGY TRANSFER; ENTEROBACTERIACEAE; FUM GENE; GLYCOLYSIS; GND GENE; MANA GENE; MARINE ENVIRONMENT; MCM GENE; METABOLIC REPROGRAMMING; METAGENOME; MICROMONAS PUSILLA; NUCLEAR REPROGRAMMING; PCC GENE; PGL GENE; PHOTOSYNTHESIS; PHOTOTROPH; PROCHLOROCOCCUS; PRS GENE; RHODOBACTERALES; RPI GENE; SALMONELLA; SDH GENE; SEA; SUNLIT OCEAN; SYNECHOCOCCUS; TALC GENE; TKT GENE; VIRUS CAPSID; VIRUS INFECTION; ZWF GENE; BACTERIOPHAGE; BACTERIUM; BIOMASS; CHROMOSOME MAP; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; GENETICS; ISOLATION AND PURIFICATION; METAGENOMICS; PHYLOGEOGRAPHY; VIROLOGY;

BACTERIA; BACTERIOPHAGES; BIOMASS; CARBON; CHROMOSOME MAPPING; ECOSYSTEM; METABOLIC NETWORKS AND PATHWAYS; METAGENOME; METAGENOMICS; MULTIGENE FAMILY; PACIFIC OCEAN; PHYLOGEOGRAPHY; RNA, RIBOSOMAL, 16S; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

EID: 84887380143     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-11-r123     Document Type: Article

References (74)

1. Falkowski PG, Barber RT, Smetacek V. Biogeochemical controls and feedbacks on ocean primary production. Science 1998, 281:200-207.
2. Kasting JF, Siefert JL. Life and the evolution of Earth's atmosphere. Science 2002, 296:1066-1068.
3. Faust K, Raes J. Microbial interactions: from networks to models. Nat Rev Microbiol 2012, 10:538-550.
4. Wright JJ, Konwar KM, Hallam SJ. Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 2012, 10:381-394.
5. Breitbart M, Thompson LR, Suttle CA, Sullivan MB. Exploring the vast diversity of marine viruses. Oceanography 2007, 20:135-139.
6. Breitbart M. Marine viruses: truth or dare. Ann Rev Mar Sci 2012, 4:425-448.
7. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 2005, 438:86-89.
8. Mann NH, Cook A, Millard A, Bailey S, Clokie M. Bacterial photosynthesis genes in a virus. Nature 2003, 424:741.
9. Millard A, Clokie MRJ, Shub DA, Mann NH. Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 2004, 101:11007-11012.
10. Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 2006, 4:e234.
11. Clokie MRJ, Shan J, Bailey S, Jia Y, Krisch HM. Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium. Environment Microbiol 2006, 8:827-835.
12. Lindell D, Penno S, Al-Qutob M, David E, Rivlin T, Lazar B, Post AF. Expression of the nitrogen stress response gene ntcA reveals nitrogen-sufficient Synechococcus populations in the oligotrophic northern Red Sea. Limnol Oceanography 2005, 50:1932-1944.
13. Bragg JG, Chisholm SW. Modelling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS One 2008, 3:e3550.
14. Hellweger FL. Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ Microbiol 2009, 11:1386-1394.
15. Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, Beja O. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environment Microbiol 2005, 7:1505-1513.
16. Koppelman R, Evans E. The metabolism of virus-infected animal cells. Prog Med Virol 1959, 2:73-105.
17. Ritter JB, Wahl AS, Freund S, Genzel Y, Reichl U. Metabolic effects of influenza virus infection in cultured animal cells: Intra- and extracellular metabolite profiling. BMC Syst Biol 2010, 4:61.
18. Janke R, Genzel Y, Wetzel M, Reichl U. Effect of influenza virus infection on key metabolic enzyme activities in MDCK cells. BMC Proc 2011, 5:P129.
19. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, Proll SC, McDermott JE, Gritsenko MA, Zhang Q, Zhao R, et al. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 2010, 6:e1000719.
20. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J, Chisholm SW. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci U S A 2011, 108:E757-E764.
21. Hurwitz BL, Sullivan MB. The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One 2013, 8:e57355.
22. Ignacio-Espinoza JC, Solonenko SA, Sullivan MB. The global virome: not as big as we thought?. Curr Opin Virol 2013, 3:566-571.
23. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, Ellisman M, Deerinck T, Sullivan MB, Giovannoni SJ. Abundant SAR11 viruses in the ocean. Nature 2013, 499:357-360.
24. Duhaime MB, Deng L, Poulos BT, Sullivan MB. Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method. Environ Microbiol 2012, 14:2526-2537.
25. John SG, Mendez CB, Deng L, Poulos B, Kauffman AKM, Kern S, Brum J, Polz MF, Boyle EA, Sullivan MB. A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ Microbiol Reports 2011, 3:195-202.
26. Hurwitz BL, Deng L, Poulos BT, Sullivan MB. Evaluation of methods to concentrate and purify ocean virus communities through comparative, replicated metagenomics. Environ Microbiol 2012, 15:1428-1440.
27. Duhaime MB, Sullivan MB. Ocean viruses: rigorously evaluating the metagenomic sample-to-sequence pipeline. Virology 2012, 434:181-186.
28. Solonenko SA, Sullivan MB. Preparation of Metagenomic Libraries from Naturally Occurring Marine Viruses. Methods in Enzymlogy: Microbial Metagenomics, Metatranscriptomics, and Metaproteomics, Volume 531 2013, 143-160. San Diego: Academic, Delong EF, 1.
29. Modi SR, Lee HH, Spina CS, Collins JJ. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 2013, 499:219-222.
30. Lang AS, Beatty JT. Importance of widespread gene transfer agent genes in alpha-proteobacteria. Trends Microbiol 2007, 15:54-62.
31. Liu B, Gibbons T, Ghodsi M, Treangen T, Pop M. Accurate and fast estimation of taxonomic profiles from metagenomic shotgun sequences. BMC Genomics 2011, 12:S4.
32. Sharon I, Battchikova N, Aro EM, Giglione C, Meinnel T, Glaser F, Pinter RY, Breitbart M, Rohwer F, Beja O. Comparative metagenomics of microbial traits within oceanic viral communities. The ISME J 2011, 5:1178-1190.
33. Luo C, Tsementzi D, Kyrpides NC, Konstantinidis KT. Individual genome assembly from complex community short-read metagenomic datasets. ISME J 2012, 6:898-901.
34. Solonenko SA, Ignacio-Espinoza JC, Alberti A, Cruaud C, Hallam S, Konstantinidis K, Tyson G, Wincker P, Sullivan MB. Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics 2013, 14:320.
35. Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M, Sarracino D, Chisholm SW. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial 'mobilome'. Environ Microbiol 2009, 11:2935-2951.
36. Huang S, Wang K, Jiao N, Chen F. Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage-host genetic exchanges. Environ Microbiol 2012, 14:540-558.
37. Sullivan MB, Huang KH, Ignacio-Espinoza JC, Berlin A, Kelly L, Weigele PR, DeFrancesco AS, Kern SE, Thompson LR, Young S, et al. Genomic analysis of oceanic cyanobacterial myoviruses compared to T4-like myoviruses from diverse hosts and environments. Environ Microbiol 2010, 12:3035-3056.
38. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 2005, 3:e144.
39. Wilson WH, Carr NG, Mann NH. The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J Phycol 1996, 32:506-516.
40. Letunic I, Yamada T, Kanehisa M, Bork P. iPath: interactive exploration of biochemical pathways and networks. Trends Biochem Sci 2008, 33:101-103.
41. Markovitz A, Sydiskis RJ, Lieberman MM. Genetic and biochemical studies on mannose-negative mutants that are deficient in phosphomannose isomerase in Escherichia coli K-12. J Bacteriol 1967, 94:1492-1496.
42. Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, Rector T, Kettler G, Sullivan MB, Steen R, Hess WR, et al. Genome-side expression dynamics of a marine virus and host reveal features of co-evolution. Nature 2007, 449:83-86.
43. Emmerling M, Dauner M, Ponti A, Fiaux J, Hochuli M, Szyperski T, Wüthrich K, Bailey JE, Sauer U. Metabolic flux responses to pyruvate kinase knockout in Escherichia coli. J Bacteriol 2002, 184:152-164.
44. Buschiazzo A, Ugalde JE, Guerin ME, Shepard W, Ugalde RA, Alzari PM. Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. EMBO J 2004, 23:3196-3205.
45. Lorenz MC, Fink GR. Life and death in a macrophage: role of the glyoxylate cycle in virulence. Eukaryot Cell 2002, 1:657-662.
46. Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM, Druffel ER, Pearson A. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci U S A 2006, 103:6442-6447.
47. Suttle CA. Viruses in the sea. Nature 2005, 437:356-361.
48. Sharon I, Tzahor S, Williamson S, Shmoish M, Man-Aharonovich D, Rusch DB, Yooseph S, Zeidner G, Golden SS, Mackey SR, et al. Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J 2007, 1:492-501.
49. Schuetz R, Zamboni N, Zampieri M, Heinemann M, Sauer U. Multidimensional optimality of microbial metabolism. Science 2012, 336:601-604.
50. Brum JR, Schenck RO, Sullivan MB. Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J 2013, 7:1738.
51. Steward GF, Culley AI, Mueller JA, Wood-Charlson EM, Belcaid M, Poisson G. Are we missing half of the viruses in the ocean?. ISME J 2013, 7:672-679.
52. Dunlap DS, Ng TF, Rosario K, Barbosa JG, Greco AM, Breitbart M, Hewson I. Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci U S A 2013, 110:1375-1380.
53. Suttle CA. Marine viruses-major players in the global ecosystem. Nat Rev Microbiol 2007, 5:801-812.
54. Allers E, Moraru C, Duhaime MB, Beneze E, Solonenko N, Barrero-Canosa J, Amann R, Sullivan MB. Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses. Environ Microbiol 2013, 15:2306.
55. Deng L, Gregory A, Yilmaz S, Poulos BT, Hugenholtz P, Sullivan MB. Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. mBio 2012, 3.
56. Tadmor AD, Ottesen EA, Leadbetter JR, Phillips R. Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 2011, 333:58-62.
57. Flores CO, Meyer JR, Valverde S, Farr L, Weitz JS. Statistical structure of host-phage interactions. Proc Natl Acad Sci U S A 2011, 108:E288-297.
58. Flores CO, Valverde S, Weitz JS. Multi-scale structure and geographic drivers of cross-infection within marine bacteria and phages. ISME J 2013, 7:520-532.
59. Weitz JS, Poisot T, Meyer JR, Flores CO, Valverde S, Sullivan MB, Hochberg ME. Phage-bacteria infection networks. Trends Microbiol 2013, 21:82-91.
60. TMPL Lab Protocols. http://eebweb.arizona.edu/Faculty/mbsulli/protocols.htm.
61. TMPL lab code. http://code.google.com/p/tmpl/downloads/list.
62. Henn MR, Sullivan MB, Stange-Thomann N, Osburne MS, Berlin AM, Kelly L, Yandava C, Kodira C, Zeng QD, Weiand M, et al. Analysis of high-throughput sequencing and annotation strategies for phage genomes. Plos One 2010, 5:e9083.
63. 454 Life Sciences. http://www.454.com.
64. CAMERA: Community Cyberinfrastructure for Advanced Microbial Ecology Research and Analysis. http://camera.calit2.net.
65. The iPlant Collaborative. http://www.iplantcollaborative.org.
66. Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma 2010, 11:119.
67. Huang Y, Niu B, Gao Y, Fu L, Li W. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 2010, 26:680-682.
68. Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K, Eisen JA, Heidelberg KB, Manning G, Li W, et al. The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol 2007, 5:e16.
69. Rattei T, Arnold R, Tischler P, Lindner D, Stumpflen V, Mewes HW. SIMAP: the similarity matrix of proteins. Nucleic Acids Res 2006, 34:D252.
70. Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, et al. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 2012, 40:D284-289.
71. Phantome: Phage Annotation Tools and Methods. http://www.phantome.org/Downloads.
72. Leplae R, Lima-Mendez G, Toussaint A. ACLAME: a CLAssification of mobile genetic elements, update 2010. Nucleic Acids Res 2010, 38:D57-D61.
73. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
74. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009, 37:D141-D145.