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Juan WANG, Yuande PENG, Zhi WANG, Wansheng ZOU, Xianjin PENG, Qisheng SONG. Transcriptional response of Microcystis aeruginosa to the recruitment promoting-benthic bacteria[J]. Journal of Oceanology and Limnology, 2022, 40(1): 153-162

Transcriptional response of Microcystis aeruginosa to the recruitment promoting-benthic bacteria
Juan WANG1, Yuande PENG2, Zhi WANG1, Wansheng ZOU3, Xianjin PENG1, Qisheng SONG4
1 College of Life Sciences, Hunan Normal University, Changsha 410081, China;
2 Institute of Bast Fiber Crops, Chinese Academy of Agricultural Sciences, Changsha 410205, China;
3 Department of Life Science, Hunan University of Arts and Science, Changde 415000, China;
4 Division of Plant Sciences, University of Missouri, Columbia 65211, MO, USA
Abstract:
Blooms of Microcystis aeruginosa occur frequently in many freshwater ecosystems around the world, but the mechanism of recovery has not been fully understood. In our previous study, three benthic bacterial species (E.sp013, Ba.spD06, and Ba.spD24) were identified capable of promoting the recruitment of M. aeruginosa. Here, we further investigated the transcriptional response of M. aeruginosa to the benthic bacteria in early phase of recruitment by means of RNA-Seq analysis. In total, 5 803 803 unigenes on average length of 404 bp were obtained from the transcriptome of M. aeruginosa. There were 54 982 unigenes identified as benthic bacteria-responsive unigenes based on the expression level analysis. Results of the protein-protein interaction analysis (PPI) show that the hub genes of the benthic bacteria responsive unigenes mediated network were ribosomal proteins of 30S and 50S, and the most significant functional module of the network was related to the ribosome. Both the unigenes encoding the translation initiation factors (IF-2, IF-3) and elongation factors (lepA, fusA, and tufA) were up-regulated to respond benthic bacteria. Therefore, it indicates that the benthic bacteria have a positive influence on activating the ribosome during the early recovery stage of M. aeruginosa.
Key words:    Microcystis aeruginosa|ribosome|benthic bacteria|chlorophyll a   
Received: 2020-10-16   Revised:
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References:
Berrendero E, Valiente E F, Perona E, Gómez C L, Loza V, Muñoz-Martín M A, Mateo P. 2016. Nitrogen fixation in a non-heterocystous cyanobacterial mat from a mountain river. Scientific Reports, 6(1): 30 920, https://doi.org/10.1038/srep30920.
Brunberg A K, Blomqvist P. 2002. Benthic overwintering of Microcystis colonies under different environmental conditions. Journal of Plankton Research, 24(11): 1 247-1 252, https://doi.org/10.1093/plankt/24.11.1247.
Buchan A, LeCleir G R, Gulvik C A, González J M. 2014. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nature Reviews Microbiology, 12(10): 686-698, https://doi.org/10.1038/nrmicro3326.
Cirés S, Wörmer L, Agha R, Quesada A. 2013. Overwintering populations of Anabaena, Aphanizomenon and Microcystis as potential inocula for summer blooms. Journal of Plankton Research, 35(6): 1 254-1 266, https://doi.org/10.1093/plankt/fbt081.
Cyr H, Curtis J M. 1999. Zooplankton community size structure and taxonomic composition affects size-selective grazing in natural communities. Oecologia, 118(3): 306-315, https://doi.org/10.1007/s004420050731.
Dokulil M, Chen W, Cai Q. 2000. Anthropogenic impacts to large lakes in China: the Tai Hu example. Aquatic Ecosystem Health and Management, 3(1): 81-94, https://doi.org/10.1016/s1463-4988(99)00067-6.
Esterhuizen-Londt M, Baik S, Kwon K S et al. 2018. Toxicity and Toxin Composition of Microcystis aeruginosa from Wangsong Reservoir. Toxicol. Environ. Health Sci., 10: 179-185, https://doi.org/10.1007/s13530-018-0362-4.
Gan N Q, Xiao Y, Zhu L, Wu Z X, Liu J, Hu C L, Song L R. 2012. The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environmental Microbiology, 14(3): 730-742, https://doi.org/10.1111/j.1462-2920.2011.02624.x.
Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q D, Chen Z H, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7): 644-652, https://doi.org/10.1038/nbt.1883.
Green R, Noller H F. 1997. Ribosomes and translation. Annual Review of Biochemistry, 66: 679-716, https://doi.org/10.1146/annurev.biochem.66.1.679.
Grossart H P, Czub G, Simon M. 2006. Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environmental Microbiology, 8(6): 1 074-1 084, https://doi.org/10.1111/j.1462-2920.2006.00999.x.
Head R M, Jones R I, Bailey-Watts A E. 1998. Akinete germination and recruitment of planktonic cyanobacteria from lake sediments. SIL Proceedings, 26(4): 1 711-1 715, https://doi.org/10.1080/03680770.1995.11901024.
Jacobson L, Halmann M. 1982. Polyphosphate metabolism in the blue-green alga Microcystis aeru-ginosa. Journal of Plankton Research, 4(3): 481-488, https://doi.org/10.1093/plankt/4.3.481.
Karlsson-Elfgren I, Rengefors K, Gustafsson S. 2004. Factors regulating recruitment from the sediment to the water column in the bloom-forming cyanobacterium Gloeotrichia echinulata. Freshwater Biology, 49(3): 265-273, https://doi.org/10.1111/j.1365-2427.2004.01182.x.
Kearns K D, Hunter M D. 2000. Green algal extracellular products regulate antialgal toxin production in a cyanobacterium. Environmental Microbiology, 2(3): 291-297, https://doi.org/10.1046/j.1462-2920.2000.00104.x.
Kruk C, Segura A M, Nogueira L, Alcantara I, Calliari D, Gabriela M D L E et al. 2017. A multilevel trait-based approach to the ecological performance of Microcystis aeruginosa complex from headwaters to the ocean. Harmful Algae, 70: 23-36, https://doi.org/10.1016/j.hal.2017.10.004.
Landa M, Blain S, Christaki U, Monchy S, Obernosterer I. 2016. Shifts in bacterial community composition associated with increased carbon cycling in a mosaic of phytoplankton blooms. ISME Journal, 10(1): 39-50, https://doi.org/10.1038/ismej.2015.105.
Li B, Dewey C N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12(1): 323, https://doi.org/10.1186/1471-2105-12-323.
Li H B, Xing P, Wu Q L L. 2012. Characterization of the bacterial community composition in a hypoxic zone induced by Microcystis blooms in Lake Taihu, China. Fems Microbiology Ecology, 79(3): 773-784, https://doi.org/10.1111/j.1574-6941.2011.01262.x.
Lin C Y, Lee T L, Chiu Y Y, Lin Y W, Lo Y S, Lin C T, Yang J M. 2015. Module organization and variance in protein-protein interaction networks. Scientific Reports, 5: 9 386, https://doi.org/10.1038/srep09386.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25(4): 402-408, https://doi.org/10.1006/meth.2001.1262.
Misson B, Donnadieu-Bernard F, Godon J J, Amblard C, Latour D. 2012. Short- and long-term dynamics of the toxic potential and genotypic structure in benthic populations of Microcystis. Water Research, 46(5): 1 438-1 446, https://doi.org/10.1016/j.watres.2011.11.011.
Mohamed Z A, Carmichael W W, Hussein A A. 2003. Estimation of microcystins in the freshwater fish Oreochromis niloticus in an Egyptian fish farm containing a Microcystis bloom. Environmental Toxicology, 18(2): 137-141, https://doi.org/10.1002/tox.10111.
Paerl H W, Bland P T, Bowles N D, Haibach N E. 1985. Adaptation to high-intensity, low-wavelength light among surface blooms of the cyanobacterium Microcystis aeruginosa. Applied and Environmental Microbiology, 49(5): 1 046-1 052, https://doi.org/10.1128/AEM.49.5.1046-1052.1985.
Parveen B, Ravet V, Djediat C, Mary I, Quiblier C, Debroas D, Humbert J F. 2013. Bacterial communities associated with Microcystis colonies differ from free-living communities living in the same ecosystem. Environmental Microbiology Reports, 5(5): 716-724, https://doi.org/10.1111/1758-2229.12071.
Pfeifer F. 2012. Distribution, formation and regulation of gas vesicles. Nature Reviews Microbiology, 10(10): 705-715, https://doi.org/10.1038/nrmicro2834.
Preston T, Stewart W D P, Reynolds C S. 1980. Bloom-forming cyanobacterium Microcystis aeruginosa overwinters on sediment surface. Nature, 288(5789): 365-367, https://doi.org/10.1038/288365a0.
Reynolds C S, Jaworski G H M. 1978. Enumeration of natural Microcystis populations. British Phycological Journal, 13(3): 269-277, https://doi.org/10.1080/00071617800650331.
Risgaard-Petersen N, Kristiansen M, Frederiksen R B, Dittmer A L, Bjerg J T, Trojan D, Schreiber L, Damgaard L R, Schramm A, Nielsen L P. 2015. Cable bacteria in freshwater sediments. Applied and Environmental Microbiology, 81(17): 6 003-6 011, https://doi.org/10.1128/aem.01064-15.
Robson B J, Hamilton D P. 2004. Three-dimensional modelling of a Microcystis bloom event in the Swan River estuary, Western Australia. Ecological Modelling, 174(1-2): 203-222, https://doi.org/10.1016/j.ecolmodel.2004.01.006.
Seebacher J, Gavin A C. 2011. SnapShot: protein-protein interaction networks. Cell, 144: 1 000-1 000.e1, https://doi.org/10.1016/j.cell.2011.02.025.
Shao K Q, Zhang L, Wang Y P, Yao X, Tang X M, Qin B Q, Gao G. 2014. The responses of the taxa composition of particle-attached bacterial community to the decomposition of Microcystis blooms. Science of the Total Environment, 488-489: 236-242, https://doi.org/10.1016/j.scitotenv.2014.04.101.
Ståhl-Delbanco A, Hansson L A, Gyllström M. 2003. Recruitment of resting stages may induce blooms of Microcystis at low N: P ratios. Journal of Plankton Research, 25(9): 1 099-1 106, https://doi.org/10.1093/plankt/25.9.1099.
Ståhl-Delbanco A, Hansson L A. 2002. Effects of bioturbation on recruitment of algal cells from the “seed bank” of lake sediments. Limnology and Oceanography, 47(6): 1 836-1 843, https://doi.org/10.4319/lo.2002.47.6.1836.
Talebi R, Ahmadi A, Afraz F. 2018. Analysis of protein-protein interaction network based on transcriptome profiling of ovine granulosa cells identifies candidate genes in cyclic recruitment of ovarian follicles. Journal of Animal Science and Technology, 60: 11, https://doi.org/10.1186/s40781-018-0171-y.
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28(5): 511-515, https://doi.org/10.1038/nbt.1621.
Trösch R, Willmund F. 2019. The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants. Biological Chemistry, 400(7): 879-893, https://doi.org/10.1515/hsz-2018-0436.
Verspagen J M H, Snelder E O F M, Visser P M, Huisman J, Mur L R, Ibelings B W. 2004. Recruitment of benthic Microcystis (Cyanophyceae) to the water column: internal buoyancy changes or resuspension? Journal of Phycology, 40(2): 260-270, https://doi.org/10.1111/j.1529-8817.2004.03174.x.
Wilson A E, Sarnelle O, Neilan B A, Salmon T P, Gehringer M M, Hay M E. 2005. Genetic variation of the bloom-forming cyanobacterium Microcystis aeruginosa within and among lakes: implications for harmful algal blooms. Applied and Environmental Microbiology, 71(10): 6 126-6 133, https://doi.org/10.1128/AEM.71.10.6126-6133.2005.
Wilson D N, Nierhaus K H. 2007. The weird and wonderful world of bacterial ribosome regulation. Critical Reviews in Biochemistry and Molecular Biology, 42(3): 187-219, https://doi.org/10.1080/10409230701360843.
Wu X D, Kong F X. 2009. Effects of light and wind speed on the vertical distribution of Microcystis aeruginosa colonies of different sizes during a summer bloom. International Review of Hydrobiology, 94(3): 258-266, https://doi.org/10.1002/iroh.200811141.
Wu Y F, Xing P, Liu S J, Wu Q L L. 2019. Enhanced microbial interactions and deterministic successions during anoxic decomposition of Microcystis biomass in lake sediment. Frontiers in Microbiology, 10: 2 474, https://doi.org/10.3389/fmicb.2019.02474.
Xing P, Guo L, Tian W, Wu Q L L. 2011. Novel Clostridium populations involved in the anaerobic degradation of Microcystis blooms. The ISME Journal, 5(5): 792-800, https://doi.org/10.1038/ismej.2010.176.
Xu L, Zhou M, Ju H Y, Zhang Z X, Zhang J Q, Sun C Y. 2018. Enterobacter aerogenes metabolites enhance Microcystis aeruginosa biomass recovery for sustainable bioflocculant and biohydrogen production. Science of The Total Environment, 634: 488-496, https://doi.org/10.1016/j.scitotenv.2018.03.327.
Yamamoto Y, Shiah F K, Chen Y L. 2011. Importance of large colony formation in bloom-forming cyanobacteria to dominate in eutrophic ponds. Annales de Limnologie-International Journal of Limnology, 47(2): 167-173, https://doi.org/10.1051/limn/2011013.
Zhou X H, Zhang J P, Wen C Z. 2017. Community composition and abundance of anammox bacteria in cattail rhizosphere sediments at three phenological stages. Current Microbiology, 74(11): 1 349-1 357, https://doi.org/10.1007/s00284-017-1324-9.
Zou W S, Wang Z, Liu L G, Wang W B, Shi Y P. 2017. Relationship between recruitment of Microcystis dormant in sediment and annual dynamics of bacterial flora in Lake Chongtian. Acta Ecologica Sinica, 37(19): 6 597-6 606. (in Chinese with English abstract)
Zou W S, Wang Z, Song Q S, Tang S X, Peng Y D. 2018. Recruitment-promoting of dormant Microcystis aeruginosa by three benthic bacterial species. Harmful Algae, 77: 18-28, https://doi.org/10.1016/j.hal.2018.05.008.
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