Photosynthetica 2021, 59(4):587-599 | DOI: 10.32615/ps.2021.050

The moderating role of population succession in the adaptive responses of Synechococcus assemblages: evidence from light intensity simulation experiment

T. WANG1, 2, 3, 4, †, X. CHEN5, †, J.L. LI1, 6, S. QIN1, 6, Y.L. CUI1, 6, F. XU2
1 Key Laboratory of Coastal Biology and Biological Resource Utilization, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, 264000 Yantai, China
2 College of Environmental Science and Engineering, Ocean University of China, 266100 Qingdao, China
3 CAS Key Laboratory for Experimental Study under Deep-sea Extreme Conditions, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, 572000 Sanya, China
4 University of Chinese Academy of Sciences, Beijing, China
5 College of Marine Life Science, Ocean University of China, 266005 Qingdao, China
6 Center for Ocean Mega-Science, Chinese Academy of Sciences, 266071 Qingdao, China

Synechococcus is one of the most abundant photoautotrophic picoplankton in the marine ecosystem. However, it is not clear how Synechococcus assemblages respond to light intensity variation in a genus group. Here, enriched Synechococcus assemblages from in situ coastal seawater were subjected to light intensity simulation experiments in a range of 9-243 μmol(photon) m-2 s-1. Characteristics concerning physiology, genomics, and metatranscriptomics were analyzed. Physiologically, the fitting model predicted photosynthesis indications and pigment contents increased with different trends following the light intensity. Genomic sequencing demonstrated that both the phylogenetic and phenotypic compositions of Synechococcus assemblage exhibited population succession. Especially, the proportion of Synechococcus pigment type 2 was changed significantly. In metatranscriptomics, most genes were downregulated in the high-light intensity group, while photosynthesis-related genes were entirely upregulated. The high upregulation of photosynthesis-related genes, such as psbO, psbA, apcB, and cpcB, corresponded to the succession of Synechococcus genotype and was responsible for the physiological shift in response to light intensity.

Additional key words: enrichment culture; genomics; irradiance; metatranscriptomics; picocyanobacteria.

Received: July 21, 2021; Revised: October 10, 2021; Accepted: October 25, 2021; Prepublished online: November 18, 2021; Published: December 17, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
WANG, T., CHEN, X., LI, J.L., QIN, S., CUI, Y.L., & XU, F. (2021). The moderating role of population succession in the adaptive responses of Synechococcus assemblages: evidence from light intensity simulation experiment. Photosynthetica, 59(4), 587-599. doi: 10.32615/ps.2021.050
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileWang_2781_supplement.docx

    File size: 865.97 kB

    References

    1. Ahlgren N.A., Rocap G.: Culture isolation and culture-independent clone libraries reveal new marine Synechococcus ecotypes with distinctive light and N physiologies. - Appl. Environ. Microb. 72: 7193-7204, 2006. Go to original source...
    2. Ahlgren N.A., Rocap G.: Diversity and distribution of marine Synechococcus: multiple gene phylogenies for consensus classification and development of qPCR assays for sensitive measurement of clades in the ocean. - Front. Microbiol. 3: 213, 2012. Go to original source...
    3. Altschul S.F., Madden T.L., Schäffer A.A. et al.: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. - Nucleic Acids Res. 25: 3389-3402, 1997. Go to original source...
    4. Bolger A.M., Lohse M., Usadel B.: Trimmomatic: a flexible trimmer for Illumina sequence data. - Bioinformatics 30: 2114-2120, 2014. Go to original source...
    5. Caporaso J.G., Kuczynski J., Stombaugh J. et al.: QIIME allows analysis of high-throughput community sequencing data. - Nat. Methods 7: 335-336, 2010. Go to original source...
    6. Chen H., Zhang D., Guo J. et al.: A Psb27 homologue in Arabidopsis thaliana is required for efficient repair of photodamaged photosystem II. - Plant Mol. Biol. 61: 567-575, 2006. Go to original source...
    7. Chin C.H., Chen S.H., Wu H.H. et al.: cytoHubba: identifying hub objects and sub-networks from complex interactome. - BMC Syst. Biol. 8: S11, 2014. Go to original source...
    8. Choi D.H., Noh J.H.: Phylogenetic diversity of Synechococcus strains isolated from the East China Sea and the East Sea. - FEMS Microbiol. Ecol. 69: 439-448, 2009. Go to original source...
    9. de Mendiburu F.: Agricolae: statistical procedures for agricultural research. R package version 1, 2014.
    10. Deng L., Ignacio-Espinoza J.C., Gregory A.C. et al.: Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. - Nature 513: 242-245, 2014. Go to original source...
    11. DuRand M.D., Olson R.J., Chisholm S.W.: Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. - Deep Sea Res. Part II Top. Stud. Oceanogr. 48: 1983-2003, 2001. Go to original source...
    12. Everroad R.C., Wood A.M.: Phycoerythrin evolution and diversification of spectral phenotype in marine Synechococcus and related picocyanobacteria. - Mol. Phylogenet. Evol. 64: 381-392, 2012. Go to original source...
    13. Flombaum P., Gallegos J.L., Gordillo R.A. et al.: Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. - P. Natl. Acad. Sci. USA 110: 9824-9829, 2013. Go to original source...
    14. Frias-Lopez J., Shi Y., Tyson G.W. et al.: Microbial community gene expression in ocean surface waters. - P. Natl. Acad. Sci. USA 105: 3805-3810, 2008. Go to original source...
    15. Fu L., Niu B., Zhu Z. et al.: CD-HIT: accelerated for clustering the next-generation sequencing data. - Bioinformatics 28: 3150-3152, 2012. Go to original source...
    16. Fuller N.J., Marie D., Partensky F. et al.: Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. - Appl. Environ. Microb. 69: 2430-2443, 2003. Go to original source...
    17. Gao X., Chen C.T.A.: Heavy metal pollution status in surface sediments of the coastal Bohai Bay. - Water Res. 46: 1901-1911, 2012. Go to original source...
    18. Gilbert J.A., Field D., Huang Y. et al.: Detection of large numbers of novel sequences in the metatranscriptomes of complex marine microbial communities. - PLoS ONE 3: e3042, 2008. Go to original source...
    19. Grébert T., Doré H., Partensky F. et al.: Light color acclimation is a key process in the global ocean distribution of Synechococcus cyanobacteria. - P. Natl. Acad. Sci. USA 115: E2010-E2019, 2018. Go to original source...
    20. Guidi L., Chaffron S., Bittner L. et al.: Plankton networks driving carbon export in the oligotrophic ocean. - Nature 532: 465-470, 2016. Go to original source...
    21. Halsey K.H., Jones B.M.: Phytoplankton strategies for photosynthetic energy allocation. - Annu. Rev. Mar. Sci. 7: 265-297, 2015. Go to original source...
    22. Hu H., Boisson-Dernier A., Israelsson-Nordström M. et al.: Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. - Nat. Cell Biol. 12: 87-93, 2010. Go to original source...
    23. Huang S., Wilhelm S.W., Harvey H.R. et al.: Novel lineages of Prochlorococcus and Synechococcus in the global oceans. - ISME J. 6: 285-297, 2012. Go to original source...
    24. Hunter-Cevera K.R., Post A.F., Peacock E.E., Sosik H.M.: Diversity of Synechococcus at the Martha's Vineyard coastal observatory: Insights from culture isolations, clone libraries, and flow cytometry. - Microb. Ecol. 71: 276-289, 2016. Go to original source...
    25. Hyatt D., LoCascio P.F., Hauser L.J., Uberbacher E.C.: Gene and translation initiation site prediction in metagenomic sequences. - Bioinformatics 28: 2223-2230, 2012. Go to original source...
    26. Jensen E.L., Clement R., Kosta A. et al.: A new widespread subclass of carbonic anhydrase in marine phytoplankton. - ISME J. 13: 2094-2106, 2019. Go to original source...
    27. Jing H., Liu H., Suzuki K.: Phylogenetic diversity of marine Synechococcus spp. in the Sea of Okhotsk. - Aquat. Microb. Ecol. 56: 55-63, 2009. Go to original source...
    28. Jod³owska S., ¦liwiñska S.: Effects of light intensity and temperature on the photosynthetic irradiance response curves and chlorophyll fluorescence in three picocyanobacterial strains of Synechococcus. - Photosynthetica 52: 223-232, 2014. Go to original source...
    29. Kanazawa H., Kayano T., Mabuchi K., Futai M.: Nucleotide sequence of the genes coding for α, β and γ subunits of the proton-translocating ATPase of Escherichia coli. - Biochem. Bioph. Res. Co. 103: 604-612, 1981. Go to original source...
    30. Kanehisa M., Goto S.: KEGG: Kyoto encyclopedia of genes and genomes. - Nucleic Acids Res. 28: 27-30, 2000. Go to original source...
    31. Klepacz-Smó³ka A., Pietrzyk D., Szel±g R. et al.: Effect of light colour and photoperiod on biomass growth and phycocyanin production by Synechococcus PCC 6715. - Bioresource Technol. 313: 123700, 2020. Go to original source...
    32. Klopfenstein D.V., Zhang L., Pedersen B.S. et al.: GOATOOLS: A Python library for Gene Ontology analyses. - Sci Rep.-UK 8: 10872, 2018. Go to original source...
    33. Kopylova E., Noé L., Touzet H.: SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. - Bioinformatics 28: 3211-3217, 2012. Go to original source...
    34. Langfelder P., Horvath S.: WGCNA: an R package for weighted correlation network analysis. - BMC Bioinformatics 9: 559, 2008. Go to original source...
    35. Lee D.J., Minchin S.D., Busby S.J.W.: Activating transcription in bacteria. - Annu. Rev. Microbiol. 66: 125-152, 2012. Go to original source...
    36. Li B., Dewey C.N.: RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. - BMC Bioinformatics 12: 323, 2011. Go to original source...
    37. Li D., Luo R., Liu C.M. et al.: MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. - Methods 102: 3-11, 2016. Go to original source...
    38. Li J., Wang T., Yu S. et al.: Community characteristics and ecological roles of bacterial biofilms associated with various algal settlements on coastal reefs. - J. Environ. Manage. 250: 109459, 2019. Go to original source...
    39. Lindell D., Post A.F.: Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea. - Limnol. Oceanogr. 40: 1130-1141, 1995. Go to original source...
    40. Liu X., Liu D., Wang Y. et al.: Temporal and spatial variations and impact factors of nutrients in Bohai Bay, China. - Mar. Pollut. Bull. 140: 549-562, 2019. Go to original source...
    41. Mackey K.R.M., Paytan A., Grossman A.R., Bailey S.: A photosynthetic strategy for coping in a high-light, low-nutrient environment. - Limnol. Oceanogr. 53: 900-913, 2008. Go to original source...
    42. Mackey K.R.M., Post A.F., McIlvin M.R., Saito M.A.: Physiological and proteomic characterization of light adaptations in marine Synechococcus. - Environ. Microbiol. 19: 2348-2365, 2017. Go to original source...
    43. Mei W., Yu G., Lai J. et al.: basicTrendline: Add trendline and confidence interval of basic regression models to plot. R package version 2, 2018.
    44. Mittal R., Tavanandi H.A., Mantri V.A., Raghavarao K.S.M.S.: Ultrasound assisted methods for enhanced extraction of phycobiliproteins from marine macro-algae, Gelidium pusillum (Rhodophyta). - Ultrason. Sonochem. 38: 92-103, 2017. Go to original source...
    45. Mühling M., Fuller N.J., Somerfield P.J. et al.: High resolution genetic diversity studies of marine Synechococcus isolates using rpoC1-based restriction fragment length poly-morphism. - Aquat. Microb. Ecol. 45: 263-275, 2006. Go to original source...
    46. Nowack S., Olsen M.T., Schaible G.A. et al.: The molecular dimension of microbial species: 2. Synechococcus strains representative of putative ecotypes inhabiting different depths in the Mushroom Spring microbial mat exhibit different adaptive and acclimative responses to light. - Front. Microbiol. 6: 626, 2015. Go to original source...
    47. Oksanen J., Blanchet F.G., Kindt R. et al.: Package 'vegan'. Community ecology package, version 2, 2013.
    48. Paulsen M.L., Doré H., Garczarek L. et al.: Synechococcus in the Atlantic gateway to the Arctic Ocean. - Front. Mar. Sci. 3: 191, 2016. Go to original source...
    49. Poretsky R.S., Sun S., Mou X., Moran M.A.: Transporter genes expressed by coastal bacterioplankton in response to dissolved organic carbon. - Environ. Microbiol. 12: 616-627, 2010. Go to original source...
    50. Roberts A., Pachter L.: Streaming fragment assignment for real-time analysis of sequencing experiments. - Nat. Methods 10: 71-73, 2013. Go to original source...
    51. Robinson M.D., McCarthy D.J., Smyth G.K.: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. - Bioinformatics 26: 139-140, 2010. Go to original source...
    52. Rocap G., Larimer F.W., Lamerdin J. et al.: Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. - Nature 424: 1042-1047, 2003. Go to original source...
    53. Scanlan D.J., Ostrowski M., Mazard S. et al.: Ecological genomics of marine picocyanobacteria. - Microbiol. Mol. Biol. Rev. 73: 249-299, 2009. Go to original source...
    54. ¦liwiñska-Wilczewska S., Konarzewska Z., Wi¶niewska K., Konik M.: Photosynthetic pigments changes of three phenotypes of picocyanobacteria Synechococcus sp. under different light and temperature conditions. - Cells 9: 2030, 2020. Go to original source...
    55. Sohm J.A., Ahlgren N.A., Thomson Z.J. et al.: Co-occurring Synechococcus ecotypes occupy four major oceanic regimes defined by temperature, macronutrients and iron. - ISME J. 10: 333-345, 2016. Go to original source...
    56. Stomp M., Huisman J., De Jongh F. et al.: Adaptive divergence in pigment composition promotes phytoplankton biodiversity. -Nature 432: 104-107, 2004. Go to original source...
    57. Sutherland C., Murakami K.S.: An introduction to the structure and function of the catalytic core enzyme of Escherichia coli RNA polymerase. - EcoSal Plus 8: 10.1128/ecosalplus.ESP-0004-2018, 2018. Go to original source...
    58. Ueno Y., Shimakawa G., Aikawa S. et al.: Photoprotection mechanisms under different CO2 regimes during photosynthesis in a green alga Chlorella variabilis. - Photosynth. Res. 144: 397-407, 2020. Go to original source...
    59. van der Hout C.M., Witbaard R., Bergman M.J.N. et al.: The dynamics of suspended particulate matter (SPM) and chlorophyll-a from intratidal to annual time scales in a coastal turbidity maximum. - J. Sea Res. 127: 105-118, 2017. Go to original source...
    60. Wagner H., Jakob T., Lavaud J., Wilhelm C.: Photosystem II cycle activity and alternative electron transport in the diatom Phaeodactylum tricornutum under dynamic light conditions and nitrogen limitation. - Photosynth. Res. 128: 151-161, 2016. Go to original source...
    61. Wang T., Chen X., Qin S., Li J.: Phylogenetic and phenogenetic diversity of Synechococcus along a Yellow Sea section reveal its environmental dependent distribution and co-occurrence microbial pattern. - J. Mar. Sci. Eng. 9: 1018, 2021. Go to original source...
    62. Xia X., Cheung S., Endo H. et al.: Latitudinal and vertical variation of Synechococcus assemblage composition along 170° W transect from the South Pacific to the Arctic Ocean. - Microb. Ecol. 77: 333-342, 2019. Go to original source...
    63. Xia X., Liu H., Choi D., Noh J.H.: Variation of Synechococcus pigment genetic diversity along two turbidity gradients in the China Seas. - Microb. Ecol. 75: 10-21, 2018. Go to original source...
    64. Zheng Q., Wang Y., Lu J. et al.: Metagenomic and metaproteomic insights into photoautotrophic and heterotrophic interactions in a Synechococcus culture. - mBio 11: e03261-19, 2020. Go to original source...
    65. Zohdi E., Abbaspour M.: Harmful algal blooms (red tide): a review of causes, impacts and approaches to monitoring and prediction. - Int. J. Environ. Sci. Technol. 16: 1789-1806, 2019. Go to original source...
    66. Zwirglmaier K., Jardillier L., Ostrowski M. et al.: Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. - Environ. Microbiol. 10: 147-161, 2008. Go to original source...

    Return to the content