Environmental proteomics of microbial plankton in a highly productive coastal upwelling system

ISME Journal

Volumn 5, Issue 5, 2011, Pages 856-865

  Sowell, Sarah M ^a   Abraham, Paul E ^b,c   Shah, Manesh ^b   Verberkmoes, Nathan C ^b   Smith, Daniel P ^a   Barofsky, Douglas F ^a   Giovannoni, Stephen J ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

metaproteomics; marine plankton; OM43 clade

Indexed keywords

BACTERIAL PROTEIN; SEA WATER;

AMINO ACID; BIOGEOCHEMISTRY; COASTAL ZONE; ENZYME ACTIVITY; GENE EXPRESSION; LIQUID CHROMATOGRAPHY; MARINE ECOSYSTEM; MASS SPECTROMETRY; METABOLISM; MICROBIAL COMMUNITY; NUTRIENT ENRICHMENT; OLIGOTROPHIC ENVIRONMENT; PROTEIN; PROTEOMICS; SURFACE WATER; UPWELLING;

ARTICLE; CLASSIFICATION; GAMMAPROTEOBACTERIA; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; PLANKTON; PROTEOMICS; ROSEOBACTER; SEA; UNITED STATES;

BACTERIAL PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GAMMAPROTEOBACTERIA; MASS SPECTROMETRY; OCEANS AND SEAS; OREGON; PLANKTON; PROTEOMICS; ROSEOBACTER; SEAWATER;

OREGON SHELF; PACIFIC OCEAN;

GAMMAPROTEOBACTERIA; MIRIDAE; ROSEOBACTER;

EID: 79955063146     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2010.168     Document Type: Article

References (52)

1. Allgaier M, Uphoff H, Felske A, Wagner-Dobler I. (2003). Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl Environ Microbiol 69:5051-5059. (Pubitemid 37150725)
2. Beja O, Suzuki MT, Heidelberg JF, Nelson KE, Preston CM, Hamada T et al. (2002). Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415:630-633. (Pubitemid 34136387)
3. Bouvier T, del Giorgio PA. (2007). Key role of selective viral-induced mortality in determining marine bacterial community composition. Environ Microbiol 9:287-297. (Pubitemid 46072118)
4. Brinkoff T, Giebel H-A, Simon M. (2008). Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189:531-539.
5. Button DK, Robertson B. (2000). Effect of nutrient kinetics and cytoarchitecture on bacterioplankter size. Limnol Oceanogr 45:499-505. (Pubitemid 30152825)
6. Cho JC, Giovannoni SJ. (2004). Cultivation and growth characteristics of a diverse group of oligotrophic marine Gammaproteobacteria. Appl Environ Microbiol 70:432-440. (Pubitemid 38090234)
7. Cho JC, Stapels MD, Morris RM, Vergin KL, Schwalbach MS, Givan sa et al. (2007). Polyphyletic photosynthetic reaction centre genes in oligotrophic marine Gammaproteobacteria. Environ Microbiol 9:1456-1463. (Pubitemid 46763526)
8. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N-U et al. (2006). Community genomics among stratified microbial assemblages in the ocean's interior. Science 311:496-503. (Pubitemid 43157723)
9. Dyhrman ST, Haley ST. (2006). Phosphorus scavenging in the unicellular marine diazotroph Crocosphaera watsonii. Appl Environ Microbiol 72:1452-1458. (Pubitemid 43271259)
10. Eng J, McCormack AL, Yates III JR. (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5:976-989.
11. Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW et al. (2008). Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105:3805-3810. (Pubitemid 351723480)
12. Fuchs BM, Spring S, Teeling H, Quast C, Wulf J, Schattenhofer M et al. (2007). Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc Natl Acad Sci USA 104:2891-2896. (Pubitemid 46331809)
13. Giovannoni SJ, Bibbs L, Cho JC, Stapels MD, Desiderio R, Vergin KL et al. (2005a). Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438:82-85. (Pubitemid 41599823)
14. Giovannoni SJ, Stingl U. (2005). Molecular diversity and ecology of microbial plankton. Nature 437:343-348. (Pubitemid 41613489)
15. Giovannoni SJ, Hayakawa DH, Tripp HJ, Stingl U, Givan SA, Cho JC et al. (2008). The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 10:1771-1782. (Pubitemid 351793619)
16. Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D et al. (2005b). Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242-1245. (Pubitemid 41170917)
17. Goericke R. (2002). Bacteriochlorophyll a in the ocean: Is anoxygenic bacterial photosynthesis important? Limnol Oceanogr 47:290-295. (Pubitemid 34115295)
18. Hoch MP, Jeffrey WH, Snyder RA, Dillon KS, Coffin RB. (2006). Expression of glutamine synthetase and glutamate dehydrogenase by marine bacterioplankton: assay optimization and efficacy for assessing nitrogen to carbon metabolic balance in situ. Limnol Oceanogr 4:308-328. (Pubitemid 351774020)
19. Kan J, Hanson TE, Ginter JM, Wang K, Chen F. (2005). Metaproteomic analysis of Chesapeake Bay microbial communities. Saline Systems 1:7.
20. Karp-Boss L, Wheeler PA, Hales B, Covert P. (2004). Distributions and variability of particulate organic matter in a coastal upwelling system. J Geophys Res 109: C09010.
21. Lee S, Fuhrman JA. (1987). Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl Environ Microbiol 53:1298-1303.
22. Lo I, Denef VJ, Verberkmoes NC, Shah MB, Goltsman D, DiBartolo G. et al. (2007). Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446:537-541. (Pubitemid 46514723)
23. Martiny AC, Coleman ML, Chisholm SW. (2006). Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103:12552-12557. (Pubitemid 44267296)
24. McDonald WH, Ohi R, Miyamoto DT, Mitchison TJ, Yates JR. (2002). Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT. 219:245-251.
25. Miller TR, Belas R. (2004). Dimethylsulfoniopropionate metabolism by Pfiesteria-associated Roseobacter spp. Appl Environ Microbiol 70:3383-3391. (Pubitemid 38745882)
26. Moran MA, Buchan A, Gonzalez JM, Heidelberg JF, Whitman WB, Kiene RP et al. (2004). Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432:910-913. (Pubitemid 40037153)
27. Moran MA, Gonzalez JM, Kiene RP. (2003). Linking a Bacterial taxon to sulfur cycling in the sea: studies of the marine Roseobacter group. Geomicrobiol J 20:375-388. (Pubitemid 37156089)
28. Morris RM, Longnecker K, Giovannoni SJ. (2006). Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom. Environ Microbiol 8:1361-1370. (Pubitemid 44025330)
29. Morris RM, Nunn BL, Frazar C, Goodlett DR, Ting YS, Rocap G. (2010). Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction. ISME J 4:673-685.
30. Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA et al. (2002). SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806-810. (Pubitemid 36019626)
31. Muller-Karger FE, Varela R, Thunell R, Luerssen R, Hu C, Walsh JJ. (2005). The importance of continental margins in the global carbon cycle. Geophys Res Lett 32: L01602.
32. Park K. (1967). Nutrient regeneration and preformed nutrients off oregon. Limnol Oceanogr 12:353-357.
33. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP. (2003). Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2:43-50. (Pubitemid 36207189)
34. Poretsky RS, Bano N, Buchan A, LeCleir G, Kleikemper J, Pickering M et al. (2005). Analysis of microbial gene transcripts in environmental samples. Appl Environ Microbiol 71:4121-4126. (Pubitemid 40980589)
35. Ram RJ, Verberkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake RC et al. (2005). Community proteomics of a natural microbial biofilm. Science 308:1915-1920. (Pubitemid 40941876)
36. Rappe MS, Vergin K, Giovannoni SJ. (2000). Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiol Ecol 33:219-232.
37. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S et al. (2007). The sorcerer II global ocean sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5: e77.
38. Scanlan DJ, Silman NJ, Donald KM, Wilson WH, Carr NG, Joint I et al. (1997). An immunological approach to detect phosphate stress in populations and single cells of photosynthetic picoplankton. Appl Environ Microbiol 63:2411-2420. (Pubitemid 27232946)
39. Sherr EB, Sherr BF, Wheeler PA. (2005). Distribution of coccoid cyanobacteria and small eukaryotic phytoplankton in the upwelling ecosystem off the Oregon coast during 2001 and 2002. Deep Sea Res Part 2 Top Stud Oceanogr 52:317-330. (Pubitemid 40323613)
40. Sowell SM, Wilhelm LJ, Norbeck AD, Lipton MS, Nicora CD, Barofsky D et al. (2008). Transport functions dominate the SAR11 metaproteome at low nutrient extremes in the Sargasso Sea. ISME J 3:93-105.
41. Steinberg DK, Carlson CA, Bates NR, Johnson RJ, Michaels AF, Knap AH. (2001). Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep-Sea Research II 48:1405-1447. (Pubitemid 32434562)
42. Stingl U, Desiderio RA, Cho JC, Vergin KL, Giovannoni SJ. (2007). The SAR92 clade: an abundant coastal clade of culturable marine bacteria possessing proteorhodopsin. Appl Environ Microbiol 73:2290-2296. (Pubitemid 46649521)
43. Tabb DL, McDonald WH, Yates III JR. (2002). DTASelect and contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 1:21-26.
44. Thompson MR, Chourey K, Froelich JM, Erickson BK, VerBerkmoes NC, Hettich RL. (2008). Experimental approach for deep proteome measurements from smallscale microbial biomass samples. 80:9517-9525.
45. Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW et al. (2005). Comparative metagenomics of microbial communities. Science 308:554-557. (Pubitemid 40570586)
46. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74. (Pubitemid 38451457)
47. Verberkmoes NC, Russell AL, Shah M, Godzik A, Rosenquist M, Halfvarson J et al. (2008). Shotgun metaproteomics of the human distal gut microbiota. ISME J 3:179-189.
48. Wheeler PA, Huyer A, Fleischbein J. (2003). Cold halocline, increased nutrients and higher chlorophyll off Oregon in 2002. Geophys Res Lett (online) 30:8021; doi:10.1029/2003GL017395.
49. Wilhelm LJ, Tripp HJ, Givan SA, Smith DP, Giovannoni SJ. (2007). Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data. Biol Direct 2:27.
50. Wu J, Sunda W, Boyle EA, Karl DM. (2000). Phosphate depletion in the western North Atlantic Ocean. Science 289:759-762. (Pubitemid 30650192)
51. Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K et al. (2007). The sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol 5: e16.
52. Zubkov MV, Sleigh MA, Burkill PH. (2000). Assaying picoplankton distribution by flow cytometry of underway samples collected along a meridional transect across the Atlantic Ocean. Aquat Microb Ecol 21:13-20. (Pubitemid 34253468)