RNA sequencing provides evidence for functional variability between naturally co-existing Alteromonas macleodii lineages

BMC Genomics

Francisco Rodriguez-Valera²  Rohit Ghai²  Eva Ausó²  Mario López-Pérez²  Nikole E Kimes¹ 

[1] Current affiliation: Department of Medicine, University of California San Francisco, 513 Parnassus Ave, San Francisco, CA 94143, USA;Evolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Apartado 18, San Juan, Alicante, 03550, , Spain

关键词: CRISPR;    Genomic islands;    Transcriptomics;    RNA-seq;    Genomic diversity;    Alteromonas macleodii;   

Others  :  1128419
DOI  :  10.1186/1471-2164-15-938

 received in 2014-01-29, accepted in 2014-10-16,  发布年份 2014

【 摘 要 】

Background

Alteromonas macleodii is a ubiquitous gammaproteobacterium shown to play a biogeochemical role in marine environments. Two A. macleodii strains (AltDE and AltDE1) isolated from the same sample (i.e., the same place at the same time) show considerable genomic differences. In this study, we investigate the transcriptional response of these two strains to varying growth conditions in order to investigate differences in their ability to adapt to varying environmental parameters.

Results

RNA sequencing revealed transcriptional changes between all growth conditions examined (e.g., temperature and medium) as well as differences between the two A. macleodii strains within a given condition. The main inter-strain differences were more marked in the adaptation to grow on minimal medium with glucose and, even more so, under starvation. These differences suggested that AltDE1 may have an advantage over AltDE when glucose is the major carbon source, and co-culture experiments confirmed this advantage. Additional differences were observed between the two strains in the expression of ncRNAs and phage-related genes, as well as motility.

Conclusions

This study shows that the genomic diversity observed in closely related strains of A. macleodii from a single environment result in different transcriptional responses to changing environmental parameters. This data provides additional support for the idea that greater diversity at the strain level of a microbial community could enhance the community’s ability to adapt to environmental shifts.

【 授权许可】

   
2014 Kimes et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]López-Pérez M, Gonzaga A, Rodriguez-Valera F: Genomic diversity of “deep ecotype” Alteromonas macleodii isolates. Evidence for pan-Mediterranean clonal frames. Genome Biol Evol 2013, 5:1220-1232.
• [2]López-Pérez M, Gonzaga A, Martin-Cuadrado A, Onyshchenko O, Ghavidel A, Ghai R, Rodriguez-Valera F: Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph. Sci Rep 2012, 2:696. doi:10.1038/srep00696
• [3]Gonzaga A, Martin-Cuadrado AB, López-Pérez M, Mizuno CM, García-Heredia I, Kimes NE, Lopez-García P, Moreira D, Ussery D, Zaballos M, Ghai R, Rodriguez-Valera F: Polyclonality of concurrent natural populations of Alteromonas macleodii. Genome Biol Evol 2012, 4:1360-1374.
• [4]García‒Martínez J, Acinas SG, Massana R, Rodríguez‒Valera F: Prevalence and microdiversity of Alteromonas macleodii‒like microorganisms in different oceanic regions. Environ Microbiol 2002, 4:42-50.
• [5]McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, Chisholm SW, DeLong EF: Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci U S A 2010, 107:16420-16427.
• [6]Baker BJ, Sheik CS, Taylor CA, Jain S, Bhasi A, Cavalcoli JD, Dick GJ: Community transcriptomic assembly reveals microbes that contribute to deep-sea carbon and nitrogen cycling. ISME J 2013, 7:1962-1973. doi:10.1038/ismej.2013.85
• [7]Acinas SG, Anton J, Rodriguez-Valera F: Diversity of free-living and attached bacteria in offshore western Mediterranean waters as depicted by analysis of genes encoding 16S rRNA. Appl Environ Microbiol 1999, 65:514-522.
• [8]Pedler BE, Aluwihare LI, Azam F: Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean. Proc Natl Acad Sci U S A 2014, 111:7202-7207.
• [9]Ivars-Martinez E, Martin-Cuadrado A-B, D'Auria G, Mira A, Ferriera S, Johnson J, Friedman R, Rodriguez-Valera F: Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J 2008, 2:1194-1212.
• [10]Tettelin H, Riley D, Cattuto C, Medini D: Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 2008, 11:472-477.
• [11]Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R: The microbial pan-genome. Curr Opin Genet Dev 2005, 15:589-594.
• [12]Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS: Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 2005, 102:13950-13955.
• [13]Chun J, Grim CJ, Hasan NA, Lee JH, Choi SY, Haley BJ, Taviani E, Jeon Y, Kim DW, Lee J, Brettin TS, Bruce DC, Challacombe JF, Detter JC, Han CS, Munk AC, Chertkov O, Meincke L, Saunders E, Walters RA, Huq A, Nair GB, Colwell RR: Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 2009, 106:15442-15447.
• [14]Conlan S, Mijares LA, Becker J, Blakesley RW, Bouffard GG, Brooks S, Coleman H, Gupta J, Gurson N, Park M: Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. Genome Biol 2012, 13:R64. BioMed Central Full Text
• [15]Lukjancenko O, Wassenaar TM, Ussery DW: Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 2010, 60:708-720.
• [16]Mira A, Martin-Cuadrado AB, D'Auria G, Rodriguez-Valera F: The bacterial pan-genome:a new paradigm in microbiology. Int Microbiol 2010, 13:45-57.
• [17]Pinto A, Melo-Barbosa H, Miyoshi A, Silva A, Azevedo V: Application of RNA-seq to reveal the transcript profile in bacteria. Genet Mol Res 2011, 10:1707-1718.
• [18]Haas BJ, Chin M, Nusbaum C, Birren BW, Livny J: How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes? BMC Genomics 2012, 13:734. BioMed Central Full Text
• [19]Deutscher MP: Chapter 9 Maturation and Degradation of Ribosomal RNA in Bacteria. In Progress in Molecular Biology and Translational Science. Volume 85. Edited by Ciaran C. San Diego: Academic Press, Elsevier; 2009::369-391.
• [20]Lopez-Perez M, Gonzaga A, Ivanova E, Rodriguez-Valera F: Genomes of Alteromonas australica, a world apart. BMC Genomics 2014, 15:483. BioMed Central Full Text
• [21]Mazel D: Integrons: agents of bacterial evolution. Nat Rev Micro 2006, 4:608-620.
• [22]Coutts G, Thomas G, Blakey D, Merrick M: Membrane sequestration of the signal transduction protein GlnK by the ammonium transporter AmtB. EMBO J 2002, 21:536-545.
• [23]Mizuno CM, Kimes NE, López-Pérez M, Ausó E, Rodriguez-Valera F, Ghai R: A Hybrid NRPS-PKS Gene Cluster Related to the Bleomycin Family of Antitumor Antibiotics in Alteromonas macleodii Strains. Plos One 2013, 8:e76021.
• [24]Scaria J, Mao C, Chen J-W, McDonough SP, Sobral B, Chang Y-F: Differential Stress Transcriptome Landscape of Historic and Recently Emerged Hypervirulent Strains of Clostridium difficile Strains Determined Using RNA-seq. Plos One 2013, 8:e78489.
• [25]Prágai Z, Harwood CR: Regulatory interactions between the Pho and σB-dependent general stress regulons of Bacillus subtilis. Microbiology 2002, 148:1593-1602.
• [26]El-Sharoud WM, Niven GW: The influence of ribosome modulation factor on the survival of stationary-phase Escherichia coli during acid stress. Microbiology 2007, 153:247-253.
• [27]Niven GW: Ribosome modulation factor protects Escherichia coli during heat stress, but this may not be dependent on ribosome dimerisation. Arch Microbiol 2004, 182:60-66.
• [28]Janosi L, Mottagui-Tabar S, Isaksson LA, Sekine Y, Ohtsubo E, Zhang S, Goon S, Nelken S, Shuda M, Kaji A: Evidence for in vivo ribosome recycling, the fourth step in protein biosynthesis. EMBO J 1998, 17:1141-1151.
• [29]Garcia-Heredia I, Martin-Cuadrado A-B, Mojica FJM, Santos F, Mira A, Antón J, Rodriguez-Valera F: Reconstructing Viral Genomes from the Environment Using Fosmid Clones: The Case of Haloviruses. Plos One 2012, 7:e33802.
• [30]Brüssow H, Canchaya C, Hardt W-D: Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 2004, 68:560-602.
• [31]Smoot LM, Smoot JC, Graham MR, Somerville GA, Sturdevant DE, Migliaccio CAL, Sylva GL, Musser JM: Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Proc Natl Acad Sci U S A 2001, 98:10416-10421.
• [32]Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J: [9] TM4 Microarray Software Suite. Methods Enzymol 2006, 411:134-193.
• [33]Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O'Toole GA: Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J Bacteriol 2009, 191:210-219.
• [34]Westra ER, Buckling A, Fineran PC: CRISPR-Cas systems: beyond adaptive immunity. Nat Rev Microbiol 2014, 12:317-326.
• [35]Repoila F, Darfeuille F: Small regulatory non‒coding RNAs in bacteria: physiology and mechanistic aspects. Biol Cell 2009, 101:117-131.
• [36]Lessa FA, Raiol T, Brigido MM, Martins Neto DS, Walter MEM, Stadler PF: Clustering Rfam 10.1: Clans, families, and classes. Genes 2012, 3:378-390.
• [37]Li L, Huang D, Cheung MK, Nong W, Huang Q, Kwan HS: BSRD: a repository for bacterial small regulatory RNA. Nucleic Acids Res 2013, 41:D233-D238.
• [38]Ellis JC, Brown JW: The RNase P family. RNA Biol 2009, 6:362-369.
• [39]Lai LB, Vioque A, Kirsebom LA, Gopalan V: Unexpected diversity of RNase P, an ancient tRNA processing enzyme: challenges and prospects. FEBS Lett 2010, 584:287-296.
• [40]Muto A, Fujihara A, Ito K, Matsuno J, Ushida C, Himeno H: Requirement of transfer‒messenger RNA for the growth of Bacillus subtilis under stresses. Genes Cells 2000, 5:627-635.
• [41]Shin J-H, Price CW: The SsrA-SmpB ribosome rescue system is important for growth of Bacillus subtilis at low and high temperatures. J Bacteriol 2007, 189:3729-3737.
• [42]Abe T, Sakaki K, Fujihara A, Ujiie H, Ushida C, Himeno H, Sato T, Muto A: tmRNA‒dependent trans‒translation is required for sporulation in Bacillus subtilis. Mol Microbiol 2008, 69:1491-1498.
• [43]Okan NA, Bliska JB, Karzai AW: A role for the SmpB-SsrA system in Yersinia pseudotuberculosis pathogenesis. PLoS Pathol 2006, 2:e6.
• [44]Himeno H, Kurita D, Muto A: tmRNA-mediated trans-translation as the major ribosome rescue system in a bacterial cell. Front Genet 2014, 5:66.
• [45]Nudler E, Mironov AS: The riboswitch control of bacterial metabolism. Trends Biochem Sci 2004, 29:11-17.
• [46]Winkler W, Nahvi A, Breaker RR: Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 2002, 419:952-956.
• [47]Lambowitz AM, Zimmerly S: Group II introns: mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 2011, 3:a003616.
• [48]López-Pérez M, Gonzaga A, Martin-Cuadrado A-B, López-García P, Rodriguez-Valera F, Kimes N: Intra- and Intergenomic Variation of Ribosomal RNA Operons in Concurrent Alteromonas macleodii Strains. Microb Ecol 2013, 65:720-730.
• [49]Rodriguez-Valera F, Martin-Cuadrado A-B, Rodriguez-Brito B, Pasic L, Thingstad TF, Rohwer F, Mira A: Explaining microbial population genomics through phage predation. Nat Rev Micro 2009, 7:828-836.
• [50]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. BioMed Central Full Text
• [51]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
• [52]Carver T, Harris SR, Otto TD, Berriman M, Parkhill J, McQuillan JA: BamView: visualizing and interpretation of next-generation sequencing read alignments. Brief Bioinform 2012, 14:203-212.