Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 47, 2016, Pages E7367-E7374

  Walworth, Nathan G ^a   Lee, Michael D ^a   Fu, Fei Xue ^a   Hutchins, David A ^a   Webb, Eric A ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

CO2; Diazotroph; Evolution; Genetic assimilation; Plasticity

Indexed keywords

CARBON DIOXIDE; NITROGEN; BACTERIAL PROTEIN; SIGMA FACTOR;

ADAPTATION; BACTERIAL GENETICS; CARBON FIXATION; CONFERENCE PAPER; CONTROLLED STUDY; CYANOBACTERIUM; ENERGY METABOLISM; ENVIRONMENTAL CHANGE; NITROGEN FIXATION; NONHUMAN; PHENOTYPE; PHENOTYPIC PLASTICITY; PHOTOAUTOTROPH; PHOTOSYNTHESIS; PHYSIOLOGICAL PROCESS; PLASTICITY; PRIORITY JOURNAL; TRANSCRIPTOMICS; TRICHODESMIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROCEDURES; REPRODUCTIVE FITNESS;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; CARBON DIOXIDE; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC FITNESS; NITROGEN; NITROGEN FIXATION; SIGMA FACTOR; TRICHODESMIUM;

EID: 84996559017     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1605202113     Document Type: Article

References (63)

1. 2-enriched ocean. Oceanography (Wash DC) 22(4):128-145.
2. Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: The problem and the evidence. Evol Appl 7(1):1-14.
3. Collins S, Rost B, Rynearson TA (2014) Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl 7(1):140-155.
4. Boyd PW, et al. (2013) Marine phytoplankton temperature versus growth responses from polar to tropical waters-outcome of a scientific community-wide study. PLoS One 8(5):e63091.
5. Schaum E, Rost B, Millar AJ, Collins S (2012) Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nat Clim Chang 3(3):298-302.
6. Draghi JA, Whitlock MC (2012) Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66(9):2891-2902.
7. Schaum C-E, Rost B, Collins S (2016) Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton. ISME J 10(1):75-84.
8. Ehrenreich IM, Pfennig DW (2016) Genetic assimilation: A review of its potential proximate causes and evolutionary consequences. Ann Bot (Lond) 117(5):769-779.
9. Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: The dynamics and genetic bases of adaptation. Nat Rev Genet 4(6):457-469.
10. Lohbeck KT, Riebesell U, Reusch TBH (2014) Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification. Proc Biol Sci 281(1786):20140003.
11. Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5(5):346-351.
12. Hutchins DA, et al. (2015) Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide. Nat Commun 6:8155.
13. Schaum CE, Collins S (2014) Plasticity predicts evolution in a marine alga. Proc Biol Sci 281(1793):20141486.
14. Travisano M, Vasi F, Lenski RE (1995) Long-term experimental evolution in Escherichia coli. III. Variation replicate populations in correlated responses to novel environments. Evolution 49(1):189-200.
15. Sañudo-Wilhelmy SA, et al. (2001) Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411(6833):66-69.
16. Mills MM, Ridame C, Davey M, La Roche J, Geider RJ (2004) Iron and phosphorus colimit nitrogen fixation in the eastern tropical North Atlantic. Nature 429(6989):292-294.
17. 2 fixation, photosynthesis, growth rates, and elemental ratios. Limnol Oceanogr 52(4):1293-1304.
18. Sohm JA, Webb EA, Capone DG (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol 9(7):499-508.
19. Chappell PD, Moffett JW, Hynes AM, Webb EA (2012) Molecular evidence of iron limitation and availability in the global diazotroph Trichodesmium. ISME J 6(9):1728-1739.
20. 2 enhances nitrogen fixation and growth in the marine cyanobacterium Trichodesmium. Glob Change Biol 13(2):531-538.
21. Barcelos E Ramos J, Biswas H, Schulz KG, LaRoche J, Riebesell U (2007) Effect of rising atmospheric carbon dioxide on the marine nitrogen fixer Trichodesmium. Global Biogeochem Cycles 21: GB2028.
22. 2-fixing cyanobacterium Trichodesmium IMS101: Physiological responses. Plant Physiol 154(1):334-345.
23. 2 concentrations. Environ Microbiol 12(7):1899-1912.
24. 2 fixation in the diazotroph Trichodesmium erythraeum (cyanobacteria). J Phycol 47(6):1292-1303.
25. 2 conditions in the western Bay of Bengal. Int J Oceanogr 2013:10.1155/2013/350465.
26. Hutchins DA, Fu F-X, Webb EA, Walworth N, Tagliabue A (2013) Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nat Geosci 6(7):1-6.
27. Langer G, Nehrke G, Probert I, Ly J, Ziveri P (2009) Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6:2637-2646.
28. Kremp A, et al. (2012) Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol 2(6):1195-1207.
29. Reusch TBH, Boyd PW (2013) Experimental evolution meets marine phytoplankton. Evolution 67(7):1849-1859.
30. Walworth N, et al. (2015) Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle. Proc Natl Acad Sci USA 112(14):4251-4256.
31. Brahamsha B, Haselkorn R (1992) Identification of multiple RNA polymerase sigma factor homologs in the cyanobacterium Anabaena sp. strain PCC 7120: Cloning, expression, and inactivation of the sigB and sigC genes. J Bacteriol 174(22):7273-7282.
32. Caslake LF, Gruber TM, Bryant DA (1997) Expression of two alternative sigma factors of Synechococcus sp. strain PCC 7002 is modulated by carbon and nitrogen stress. Microbiology 143(Pt 12):3807-3818.
33. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550.
34. Imamura S, Asayama M (2009) Sigma factors for cyanobacterial transcription. Gene Regul Syst Bio 3:65-87.
35. Camsund D, Lindblad P (2014) Engineered transcriptional systems for cyanobacterial biotechnology. Front Bioeng Biotechnol 2(Suppl.):40.
36. López-Gomollón S, et al. (2007) Cross-talk between iron and nitrogen regulatory networks in Anabaena (Nostoc) sp. PCC 7120: Identification of overlapping genes in FurA and NtcA regulons. J Mol Biol 374(1):267-281.
37. González A, Bes MT, Valladares A, Peleato ML, Fillat MF (2012) FurA is the master regulator of iron homeostasis and modulates the expression of tetrapyrrole biosynthesis genes in Anabaena sp. PCC 7120. Environ Microbiol 14(12):3175-3187.
38. Wu LJ, Errington J (2000) Identification and characterization of a new presporespecific regulatory gene, rsfA, of Bacillus subtilis. J Bacteriol 182(2):418-424.
39. Su Z, Olman V, Xu Y (2007) Computational prediction of Pho regulons in cyanobacteria. BMC Genomics 8(1):156.
40. Pawlowski K, Klosse U, De Bruijn FJ (1991) Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism. Mol Gen Genet 231(1):124-138.
41. Narikawa R, Okamoto S, Ikeuchi M, Ohmori M (2004) Molecular evolution of PAS domain-containing proteins of filamentous cyanobacteria through domain shuffling and domain duplication. DNA Res 11(2):69-81.
42. Ashby MK, Houmard J (2006) Cyanobacterial two-component proteins: Structure, diversity, distribution, and evolution. Microbiol Mol Biol Rev 70(2):472-509.
43. Iranzo J, Gómez MJ, López De Saro FJ, Manrubia S (2014) Large-scale genomic analysis suggests a neutral punctuated dynamics of transposable elements in bacterial genomes. PLOS Comput Biol 10(6):e1003680.
44. Treangen TJ, Salzberg SL (2012) Repetitive DNA and next-generation sequencing: Computational challenges and solutions. Nat Rev Genet 13(1):36-46.
45. Suzuki R, Shimodaira H (2006) Pvclust: An R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22(12):1540-1542.
46. Navarro-Quezada A, Schoen DJ (2002) Sequence evolution and copy number of Ty1-copia retrotransposons in diverse plant genomes. Proc Natl Acad Sci USA 99(1):268-273.
47. Delihas N (2011) Impact of small repeat sequences on bacterial genome evolution. Genome Biol Evol 3(0):959-973.
48. Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13(4):227-232.
49. Kronholm I, Collins S (2016) Epigenetic mutations can both help and hinder adaptive evolution. Mol Ecol 25(8):1856-1868.
50. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209(Pt 12):2362-2367.
51. Tang X-S, et al. (1994) Identification of histidine at the catalytic site of the photosynthetic oxygen-evolving complex. Proc Natl Acad Sci USA 91(2):704-708.
52. Onidas D, Stachnik JM, Brucker S, Krätzig S, Gerwert K (2010) Histidine is involved in coupling proton uptake to electron transfer in photosynthetic proteins. Eur J Cell Biol 89(12):983-989.
53. Walworth NG, et al. (2016) Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean. Nat Commun 7:12081.
54. Reusch TBH (2014) Climate change in the oceans: Evolutionary versus phenotypically plastic responses of marine animals and plants. Evol Appl 7(1):104-122.
55. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357-359.
56. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139-140.
57. Heberle H, Meirelles GV, Da Silva FR, Telles GP, Minghim R (2015) InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics 16(1):169.
58. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. JRStat Soc B 57(1):289-300.
59. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460-2461.
60. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403-410.
61. Prufert-Bebout L, Paerl HW, Lassen C (1993) Growth, nitrogen fixation, and spectral attenuation in cultivated Trichodesmium species. Appl Environ Microbiol 59(5):1367-1375.
62. Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11(3):R25.
63. Nookaew I, et al. (2012) A comprehensive comparison of RNA-Seq-based transcriptome analysis from reads to differential gene expression and cross-comparison with microarrays: a case study in Saccharomyces cerevisiae. Nucleic Acids Res 40(20):10084-10097.