Nitrogen cost minimization is promoted by structural changes in the transcriptome of N-deprived Prochlorococcus cells

ISME Journal

Volumn 11, Issue 10, 2017, Pages 2267-2278

  Read, Robert W ^a   Berube, Paul M ^b   Biller, Steven J ^b   Neveux, Iva ^a   Cubillos Ruiz, Andres ^b,c   Chisholm, Sallie W ^b,c   Grzymski, Joseph J ^a  

^a DESERT RESEARCH INSTITUTE   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; AMINO ACID; CELLS AND CELL COMPONENTS; CYANOBACTERIUM; GENE; GENE EXPRESSION; GROWTH; MOLECULAR ANALYSIS; NITROGEN; NUTRIENT LIMITATION; PROTEIN;

PROCHLOROCOCCUS;

NITROGEN; TRANSCRIPTOME;

GENETICS; METABOLISM; PROCHLOROCOCCUS; TRANSCRIPTION INITIATION SITE;

NITROGEN; PROCHLOROCOCCUS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTOME;

EID: 85029652842     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2017.88     Document Type: Article

References (56)

1. Ahlgren NA, Rocap G, Chisholm SW. (2006). Measurement of Prochlorococcus ecotypes using real-time polymerase chain reaction reveals different abundances of genotypes with similar light physiologies. Environ Microbiol 8: 441-454.
2. Amman F, Wolfinger MT, Lorenz R, Hofacker IL, Stadler PF, Findeiß S. (2014). TSSAR: TSS annotation regime for dRNA-seq data. BMC Bioinformatics 15: 89.
3. Anders S, Huber W. (2010). Differential expression analysis for sequence count data. Genome Biol 11: R106.
4. Andrews S. (2010). FastQC: a quality control tool for high throughput sequence data. Available online at: http:// www. bioinformatics. babraham. ac. uk/projects/fastqc.
5. Baudouin-Cornu P, Surdin-Kerjan Y, Marlière P, Thomas D. (2001). Molecular evolution of protein atomic composition. Science 293: 297-300.
6. Benjamini Y, Hochberg Y. (1995). Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc B 57: 289-300.
7. Bibby TS, Mary I, Nield J, Partensky F, Barber J. (2003). Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature 424: 1051-1054.
8. Cavender-Bares KK, Mann EL, Chisholm SW, Ondrusek ME, Bidigare RR. (1999). Differential response of equatorial Pacific phytoplankton to iron fertilization. Limnol Oceanogr 44: 237-246.
9. Celesnik H, Deana A, Belasco JG. (2007). Initiation of RNA decay in Escherichia coli by 5 pyrophosphate removal. Mol Cell 27: 79-90.
10. Chisholm SW. (1992). Phytoplankton Size. In: Falkowski PG, Woodhead AD (eds). Primary Productivity and Biogeochemical Cycles in the Sea. Springer, US: Boston, MA, USA pp 213-237.
11. Deutsch C, Sarmiento JL, Sigman DM, Gruber N, Dunne JP. (2007). Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445: 163-167.
12. Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N et al. (2013). Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci USA 110: 9824-9829.
13. Gavis J. (1976). Munk and Riley revisited-Nutrient diffusion transport and rates of phytoplankton growth. J Mar Res 34: 161-179.
14. Gilbert JDJ, Fagan WF. (2011). Contrasting mechanisms of proteomic nitrogen thrift in Prochlorococcus. Mol Ecol 20: 92-104.
15. Giovannoni SJ, Thrash JC, Temperton B. (2014). Implications of streamlining theory for microbial ecology. ISME J 8: 1553-1565.
16. Grzymski JJ, Dussaq AM. (2012). The significance of nitrogen cost minimization in proteomes of marine microorganisms. ISME J 6: 71-80.
17. Grzymski JJ, Marsh AG. (2014). Protein languages differ depending on microorganism lifestyle. Ouzounis CA (ed) PLoS One 9: e96910.
18. Havaux M, Guedeney G, He Q, Grossman AR. (2003). Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. BBA Bioenerg 1557: 21-33.
19. Hoffmann S, Otto C, Doose G, Tanzer A, Langenberger D, Christ S et al. (2014). A multi-split mapping algorithm for circular RNA, splicing, trans-splicing and fusion detection. Genome Biol 15: R34.
20. Hoffmann S, Otto C, Kurtz S, Sharma CM, Khaitovich P, Vogel J et al. (2009). Fast mapping of short sequences with mismatches, insertions and deletions using index structures. Searls DB (ed) PLoS Comput Biol 5: e1000502.
21. Li G-W, Oh E, Weissman JS. (2012). The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484: 538-541.
22. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
23. Lybecker M, Bilusic I, Raghavan R. (2014). Pervasive transcription: detecting functional RNAs in bacteria. Transcription 5: e944039.
24. Malmstrom RR, Coe A, Kettler GC, Martiny AC, Frias-Lopez J, Zinser ER et al. (2010). Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J 4: 1252-1264.
25. McClure R, Balasubramanian D, Sun Y, Bobrovskyy M, Sumby P, Genco CA et al. (2013). Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res 41: e140-e140.
26. Mezulis S, Yates CM, Wass MN, Sternberg MJE, Kelley LA. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10: 845-858.
27. Mitschke J, Georg J, Scholz I, Sharma CM, Dienst D, Bantscheff J et al. (2011). An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci USA 108: 2124-2129.
28. Moll I, Grill S, Gualerzi CO, Bläsi U. (2002). Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 43: 239-246.
29. Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW et al. (2013). Processes and patterns of oceanic nutrient limitation. Nat Geosci 6: 701-710.
30. Moore LR, Coe A, Zinser ER, Saito MA, Sullivan MB, Lindell D et al. (2007). Culturing the marine cyanobacterium Prochlorococcus. Limnol Oceanogr Met 5: 353-362.
31. Munk WH, Riley GA. (1952). Absorption of nutrients by aquatic plants. J Mar Res 11: 215-240.
32. Mutsuda M, Sugiura M. (2006). Translation initiation of cyanobacterial rbcS mRNAs requires the 38-kDa ribosomal protein S1 but not the Shine-Dalgarno sequence: development of a cyanobacterial in vitro translation system. J Biol Chem 281: 38314-38321.
33. Ohashi Y, Shi W, Takatani N, AichiM, Maeda S-I, Watanabe S et al. (2011). Regulation of nitrate assimilation in cyanobacteria. J Exp Bot 62: 1411-1424.
34. Olson RJ, Vaulot D, Chisholm SW. (1985). Marine phytoplankton distributions measured using shipboard flow cytometry. DeepSea Res 32: 1273-1280.
35. Parkhill JP, Maillet G, Cullen JJ. (2001). Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37: 517-529.
36. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G et al. (2011). Integrative genomics viewer. Nat Biotech 29: 24-26.
37. Sauer J, GörlM, Forchhammer K. (1999). Nitrogen starvation in Synechococcus PCC 7942: involvement of glutamine synthetase and NtcA in phycobiliprotein degradation and survival. Arch Microbiol 172: 247-255.
38. Schoenberg DR. (2007). The end defines the means in bacterial mRNA decay. Nat Chem Biol 3: 535-536.
39. Shao W, PriceMN, Deutschbauer AM, RomineMF, Arkin AP. (2014). Conservation of transcription start sites within genes across a bacterial genus. MBio 5: e01398-14-e01398-14.
40. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiß S, Sittka A et al. (2010). The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
41. Sherman MY, Qian S-B. (2013). Less is more: improving proteostasis by translation slow down. Trends Biochem Sci 38: 585-591.
42. Sowell SM, Wilhelm LJ, Norbeck AD, Lipton MS, Nicora CD, Barofsky DF et al. (2008). Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J 3: 93-105.
43. Steglich C, Futschik ME, Lindell D, Voss B, Chisholm SW, Hess WR. (2008). The challenge of regulation in a minimal photoautotroph: non-coding RNAs in Prochlorococcus. PLoS Genet 4: e1000173.
44. Steglich C, Lindell D, Futschik M, Rector T, Steen R, Chisholm SW. (2010). Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus. Genome Biol 11: R54.
45. Su Z. (2005). Comparative genomics analysis of NtcA regulons in cyanobacteria: regulation of nitrogen assimilation and its coupling to photosynthesis. Nucleic Acids Res 33: 5156-5171.
46. Thomason MK, Bischler T, Eisenbart SK, Förstner KU, Zhang A, Herbig A et al. (2015). Global transcriptional start site mapping using differential RNA sequencing reveals novel antisense RNAs in Escherichia coli. J Bacteriol 197: 18-28.
47. Thompson AW, Huang K, Saito MA, Chisholm SW. (2011). Transcriptome response of high-and low-light-adapted Prochlorococcus strains to changing iron availability. ISME J 5: 1580-1594.
48. Thorvaldsdóttir H, Robinson JT, Mesirov JP. (2013). Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14: 178-192.
49. Tjaden B. (2015). De novo assembly of bacterial transcriptomes from RNA-seq data. Genome Biol 16: 1.
50. Tolonen AC, Aach J, Lindell D, Johnson ZI, Rector T, Steen R et al. (2006). Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Syst Biol 2: 53.
51. Tyrrell T. (1999). The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400: 525-531.
52. Van Mooy BAS, Rocap G, Fredricks HF, Evans CT, Devol AH. (2006). Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103: 8607-8612.
53. Voigt K, Sharma CM, Mitschke J, Lambrecht SJ, Voß B, Hess WR et al. (2014). Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity. ISME J 8: 2056-2068.
54. Wickham H. (2009). ggplot2: elegant graphics for data analysis. Springer: New York.
55. Zinser ER, Coe A, Johnson ZI, Martiny AC, Fuller NJ, Scanlan DJ et al. (2006). Prochlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improved quantitative PCR method. Appl Environ Microbiol 72: 723-732.
56. Zinser ER, Johnson ZI, Coe A, Karaca E, Veneziano D, Chisholm SW. (2007). Influence of light and temperature on Prochlorococcus ecotype distributions in the Atlantic Ocean. Limnol and Oceanogr 52: 2205-2220.