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Discovering Trends in Environmental Time-Series with Supervised Classification of Metatranscriptomic Reads and Empirical Mode Decomposition

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Biomedical Engineering Systems and Technologies (BIOSTEC 2018)

Abstract

In metagenomic and metatranscriptomic studies, the assignment of reads to taxonomic bins is typically performed by sequence similarity or phylogeny based approaches. Such methods become less effective if the sequences are closely related and/or of limited length. Here, we propose an approach for multi-class supervised classification of metatranscriptomic reads of short length (100–300 bp) which exploits k-mers frequencies as discriminating features. In addition, we take a first step in addressing the lack of established methods for the analysis of periodic features in environmental time-series by proposing Empirical Mode Decomposition as a way of extracting information on heterogeneity and population dynamics in natural microbial communities. To prove the validity of our computational approach as an effective tool to generate new biological insights, we applied it to investigate the transcriptional dynamics of viral infection in the ocean. We used data extracted from a previously published metatranscriptome profile of a naturally occurring oceanic bacterial assemblage sampled Lagrangially over 3 days. We discovered the existence of light-dark oscillations in the expression patterns of auxiliary metabolic genes in cyanophages which follow the harmonic diel transcription of both oxygenic photoautotrophic and heterotrophic members of the community, in agreement to what other studies have just recently found. Our proposed methodology can be extended to many other datasets opening opportunities for a better understanding of the structure and function of microbial communities in their natural environment.

E. Acerbi and C. Chénard—Contributed equally.

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References

  1. Acerbi, E., Chenard, C., Schuster, S.C., Lauro, F.M.: Supervised classification of metatranscriptomic reads reveals the existence of light-dark oscillations during infection of phytoplankton by viruses. In: Proceedings of the 11th International Joint Conference on Biomedical Engineering Systems and Technologies (BIOSTEC 2018) - Volume 3: BIOINFORMATICS, Funchal, Madeira, Portugal, 19–21 January 2018, pp. 69–77 (2018). https://doi.org/10.5220/0006763200690077

  2. Aylward, F.O., et al.: Diel cycling and long-term persistence of viruses in the Ocean’s euphotic zone. Proc. Natl. Acad. Sci. 114(43), 11446–11451 (2017)

    Article  Google Scholar 

  3. Bagherzadeh, S.A., Sabzehparvar, M.: A local and online sifting process for the empirical mode decomposition and its application in aircraft damage detection. Mech. Syst. Signal Process. 54, 68–83 (2015)

    Article  Google Scholar 

  4. de Bashan, L.E., Trejo, A., Huss, V.A., Hernandez, J.P., Bashan, Y.: Chlorella sorokiniana utex 2805, a heat and intense, sunlight-tolerant microalga with potential for removing ammonium from wastewater. Bioresour. Technol. 99(11), 4980–4989 (2008)

    Article  Google Scholar 

  5. Breitbart, M., Thompson, L.R., Suttle, C.A., Sullivan, M.: Exploring the vast diversity of marine viruses. Oceanography 20(SPL. ISS. 2), 135–139 (2007)

    Article  Google Scholar 

  6. Chambers, D.P.: Evaluation of empirical mode decomposition for quantifying multi-decadal variations and acceleration in sea level records. Nonlinear Process. Geophys. 22(2), 157–166 (2015)

    Article  Google Scholar 

  7. Chang, C.C., Lin, C.J.: LIBSVM: a library for support vector machines. ACM Trans. Intell. Syst. Technol. 2, 27:1–27:27 (2011)

    Article  Google Scholar 

  8. Chang, K.M.: Ensemble empirical mode decomposition for high frequency ECG noise reduction. Biomed. Tech./Biomed. Eng. 55(4), 193–201 (2010)

    Article  Google Scholar 

  9. Chen, C.R., Shu, W.Y., Chang, C.W., Hsu, I.C.: Identification of under-detected periodicity in time-series microarray data by using empirical mode decomposition. PLoS ONE 9(11), e111719 (2014)

    Article  Google Scholar 

  10. Chen, Y., Wei, D., Wang, Y., Zhang, X.: The role of interactions between bacterial chaperone, aspartate aminotransferase, and viral protein during virus infection in high temperature environment: the interactions between bacterium and virus proteins. BMC Microbiol. 13(1), 48 (2013)

    Article  Google Scholar 

  11. Chenard, C., Suttle, C.A.: Phylogenetic diversity of sequences of cyanophage photosynthetic gene psbA in marine and freshwaters. Appl. Environ. Microbiol. 74(17), 5317–5324 (2008)

    Article  Google Scholar 

  12. Clokie, M.R., Millard, A.D., Mehta, J.Y., Mann, N.H.: Virus isolation studies suggest short-term variations in abundance in natural cyanophage populations of the indian ocean. J. Mar. Biol. Assoc. U. K. 86(03), 499–505 (2006)

    Article  Google Scholar 

  13. Clokie, M.R., et al.: Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium. Environ. Microbiol. 8(5), 827–835 (2006)

    Article  Google Scholar 

  14. Cole, J.J.: Interactions between bacteria and algae in aquatic ecosystems. Annu. Rev. Ecol. Syst. 13(1), 291–314 (1982)

    Article  Google Scholar 

  15. Doron, S., et al.: Transcriptome dynamics of a broad host-range cyanophage and its hosts. The ISME J. 10(6), 1437 (2016)

    Article  Google Scholar 

  16. Frees, D., et al.: CLP atpases are required for stress tolerance, intracellular replication and biofilm formation in staphylococcus aureus. Mol. Microbiol. 54(5), 1445–1462 (2004)

    Article  Google Scholar 

  17. Golden, S.S., Ishiura, M., Johnson, C.H., Kondo, T.: Cyanobacterial circadian rhythms. Annu. Rev. Plant Biol. 48(1), 327–354 (1997)

    Article  Google Scholar 

  18. Goldsmith, D.B., et al.: Development of phoh as a novel signature gene for assessing marine phage diversity. Appl. Environ. Microbiol. 77(21), 7730–7739 (2011)

    Article  Google Scholar 

  19. Goldsmith, D.B., Parsons, R.J., Beyene, D., Salamon, P., Breitbart, M.: Deep sequencing of the viral phoH gene reveals temporal variation, depth-specific composition, and persistent dominance of the same viral phoh genes in the sargasso sea. PeerJ 3, e997 (2015)

    Article  Google Scholar 

  20. Hahnke, S., Brock, N.L., Zell, C., Simon, M., Dickschat, J.S., Brinkhoff, T.: Physiological diversity of roseobacter clade bacteria co-occurring during a phytoplankton bloom in the north sea. Syst. Appl. Microbiol. 36(1), 39–48 (2013)

    Article  Google Scholar 

  21. Han, J., van der Baan, M.: Empirical mode decomposition for seismic time-frequency analysis. Geophysics 78(2), O9–O19 (2013)

    Article  Google Scholar 

  22. Hess, W.R.: Genome analysis of marine photosynthetic microbes and their global role. Curr. Opin. Biotechnol. 15(3), 191–198 (2004)

    Article  Google Scholar 

  23. Holmfeldt, K., et al.: Twelve previously unknown phage genera are ubiquitous in global oceans. Proc. Natl. Acad. Sci. 110(31), 12798–12803 (2013)

    Article  Google Scholar 

  24. Huang, N.E., et al.: The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis. In: Proceedings of the Royal Society of London A: Mathematical, Physical and Engineering Sciences, vol. 454, pp. 903–995. The Royal Society (1998)

    Google Scholar 

  25. Kim, D., Oh, H.S.: EMD: a package for empirical mode decomposition and Hilbert spectrum. R J. 1(1), 40–46 (2009)

    Article  Google Scholar 

  26. Kurochkina, L.P., Semenyuk, P.I., Orlov, V.N., Robben, J., Sykilinda, N.N., Mesyanzhinov, V.V.: Expression and functional characterization of the first bacteriophage-encoded chaperonin. J. Virol. 86(18), 10103–10111 (2012)

    Article  Google Scholar 

  27. Lauro, F.M., et al.: The genomic basis of trophic strategy in marine bacteria. Proc. Natl. Acad. Sci. 106(37), 15527–15533 (2009)

    Article  Google Scholar 

  28. Li, F., Jo, Y.H., Liu, W.T., Yan, X.H.: A dipole pattern of the sea surface height anomaly in the north Atlantic: 1990s–2000s. Geophys. Res. Lett. 39(15) (2012)

    Google Scholar 

  29. Lindell, D., et al.: Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449(7158), 83–86 (2007)

    Article  Google Scholar 

  30. Liu, R., Chen, Y., Zhang, R., Liu, Y., Jiao, N., Zeng, Q.: Cyanophages exhibit rhythmic infection patterns under light-dark cycles. bioRxiv p. 167650 (2017)

    Google Scholar 

  31. Mayali, X., Franks, P.J., Azam, F.: Cultivation and ecosystem role of a marine roseobacter clade-affiliated cluster bacterium. Appl. Environ. Microbiol. 74(9), 2595–2603 (2008)

    Article  Google Scholar 

  32. Mella-Flores, D., et al.: Prochlorococcus and synechococcus have evolved different adaptive mechanisms to cope with light and UV stress (2012)

    Google Scholar 

  33. Mourino-Pérez, R.R., Worden, A.Z., Azam, F.: Growth of vibrio cholerae o1 in red tide waters off california. Appl. Environ. Microbiol. 69(11), 6923–6931 (2003)

    Article  Google Scholar 

  34. Ni, T., Zeng, Q.: Diel infection of cyanobacteria by cyanophages. Front. Mar. Sci. 2, 123 (2016)

    Article  Google Scholar 

  35. Ottesen, E.A., et al.: Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science 345(6193), 207–212 (2014)

    Article  Google Scholar 

  36. Partensky, F., Hess, W.R., Vaulot, D.: Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63(1), 106–127 (1999)

    Google Scholar 

  37. Paulson, J.N., Stine, O.C., Bravo, H.C., Pop, M.: Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10(12), 1200–1202 (2013)

    Article  Google Scholar 

  38. Ribalet, F., et al.: Light-driven synchrony of prochlorococcus growth and mortality in the subtropical Pacific gyre. Proc. Natl. Acad. Sci. 112(26), 8008–8012 (2015)

    Article  Google Scholar 

  39. Sandberg, R., Winberg, G., Bränden, C.I., Kaske, A., Ernberg, I., Cöster, J.: Capturing whole-genome characteristics in short sequences using a Naive Bayesian classifier. Genome Res. 11(8), 1404–1409 (2001)

    Article  Google Scholar 

  40. Stitson, M., Weston, J., Gammerman, A., Vovk, V., Vapnik, V.: Theory of support vector machines. Technical report, CSD-TR-96-17, Computational Intelligence Group, University of London (1996)

    Google Scholar 

  41. Sullivan, M.B., Lindell, D., Lee, J.A., Thompson, L.R., Bielawski, J.P., Chisholm, S.W.: Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol. 4(8), e234 (2006)

    Article  Google Scholar 

  42. Sullivan, M.B., Waterbury, J.B., Chisholm, S.W.: Cyanophages infecting the oceanic cyanobacterium prochlorococcus. Nature 424(6952), 1047–1051 (2003)

    Article  Google Scholar 

  43. Suttle, C.A., Chen, F.: Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58(11), 3721–3729 (1992)

    Google Scholar 

  44. Thompson, L.R., et al.: Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc. Natl. Acad. Sci. 108(39), E757–E764 (2011)

    Article  Google Scholar 

  45. Tolonen, A.C., et al.: Global gene expression of prochlorococcus ecotypes in response to changes in nitrogen availability. Mol. Syst. Biol. 2(1), 53 (2006)

    Article  Google Scholar 

  46. Tzahor, S., et al.: A supervised learning approach for taxonomic classification of core-photosystem-II genes and transcripts in the marine environment. BMC Genom. 10(1), 229 (2009)

    Article  Google Scholar 

  47. Wilhelm, S.W., Weinbauer, M.G., Suttle, C.A., Jeffrey, W.H.: The role of sunlight in the removal and repair of viruses in the sea. Limnol. Ocean. 43(4), 586–592 (1998)

    Article  Google Scholar 

  48. Wyckoff, T.J., Taylor, J.A., Salama, N.R.: Beyond growth: novel functions for bacterial cell wall hydrolases. Trends Microbiol. 20(11), 540–547 (2012)

    Article  Google Scholar 

  49. Zhao, Y., Tang, H., Ye, Y.: RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing data. Bioinformatics 28(1), 125–126 (2011)

    Article  Google Scholar 

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Acknowledgements

The authors would like to acknowledge financial support from Singapore’s Ministry of Education Academic Research Fund Tier 3 under the research grant MOE2013-T3-1-013, Singapore’s National Research Foundation under its Marine Science Research and Development Programme (Award No. MSRDP-P13) and the Singapore Centre for Environmental Life Sciences Engineering (SCELSE), whose research is supported by the National Research Foundation Singapore, Ministry of Education, Nanyang Technological University and National University of Singapore, under its Research Centre of Excellence Program. The authors would like to thank Fabio Stella, Rohan Williams and James Houghton for their valuable feedbacks.

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Acerbi, E., Chénard, C., Schuster, S.C., Lauro, F.M. (2019). Discovering Trends in Environmental Time-Series with Supervised Classification of Metatranscriptomic Reads and Empirical Mode Decomposition. In: Cliquet Jr., A., et al. Biomedical Engineering Systems and Technologies. BIOSTEC 2018. Communications in Computer and Information Science, vol 1024. Springer, Cham. https://doi.org/10.1007/978-3-030-29196-9_11

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  • DOI: https://doi.org/10.1007/978-3-030-29196-9_11

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