Academic Scientific JournalsEpiphytic bacterial community composition on the surface of the submerged macrophyte Myriophyllum spicatum in a low-salinity sea area of Hangzhou Bay
Keywords:
Myriophyllum spicatum, epiphytic bacteria, Hangzhou Bay, bacterioplankton, sedimentAbstract
In this study, we conducted a comparative analysis of the abundance and diversity of bacteria on the surface of the submerged macrophyte Myriophyllum spicatum, as well as in the surrounding water column and sediment in the low-salinity area of Hangzhou Bay, China. Bacterial clones from three clone libraries were classified into 2089 operational taxonomic units (OTUs), most of which affiliated with bacterial divisions commonly found in marine ecosystems. Alphaproteobacteria, Cyanobacteria and Gammaproteobacteria were the most abundant groups of bacteria on the surface of plants, in the water column and sediment, respectively. Epiphytic bacterial communities were more closely related to those in the sediment than bacterioplankton, and some species of epiphytic bacteria were found only on the surface of M. spicatum. The relative abundance of epiphytic bacterial genera associated with breakdown of organic compounds and with cellulose digestion was higher in October than that in July. These results suggested that bacterial communities on the surface of M. spicatum may originate from sediment bacterial communities and their specific structure was gradually formed on the surface of M. spicatum after being cultivated in low-salinity seawater.
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Albakosh, M.A., Naidoo, R.K. & Kirby, B. (2015). Identification of epiphytic bacterial communities associated with the brown alga Splachnidium rugosum. J. Appl. Phycol. 28(3): 1891–1901. DOI: 10.1007/s10811-015-0725-z.
Bowen, J.L., Ward, B.B. & Morrison, H.G. (2011). Microbial community composition in sediments resists perturbation by nutrient enrichment. Isme Journal 5(9): 1540–1548. DOI: 10.1038/ismej.2011.22.
Buesing, N., Filippini, M. & Bürgmann, H. (2009). Microbial communities in contrasting freshwater marsh microhabitats. Fems Microbiol. Ecol. 69(1): 84–97. DOI: 10.1111/j.1574-6941.2009.00692.x.
Burke, C., Thomas, T. & Lewis, M. (2011). Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. Isme Journal 5(4): 590–600. DOI: 10.1038/ismej.2010.164.
Cai, X., Gao, G. & Yang, J. (2014). An ultrasonic method for separation of epiphytic microbes from freshwater submerged macrophytes. J. Basic Microb. 54(7): 758–761. DOI: 10.1002/jobm.201300041.
Compant, S., Clément, C. & Sessitsch, A. (2010). Plant growthpromoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biology & Biochemistry 42(5): 669–678. DOI: 10.1016/j.soilbio.2009.11.024.
Crump, B.C. & Koch, E.W. (2008). Attached bacterial populations shared by four species of aquatic angiosperms. Appl. Environ. Microbiol. 74(19): 5948–5957. DOI: 10.1128/AEM.00952-08.
Dimitriu, P.A., Pinkart, H.C. & Peyton, B.M. (2008). Spatial and Temporal Patterns in the Microbial Diversity of a Meromictic Soda Lake in Washington State. Appl. Environ. Microbiol. 74(15): 4877–4888. DOI: 10.1128/AEM.00455-08.
Fan, Z., Han, R.M. & Ma, J. (2016). Submerged macrophytes shape the abundance and diversity of bacterial denitrifiers in bacterioplankton and epiphyton in the Shallow Fresh Lake Taihu, China. Environmental Science & Pollution Research 23(14): 14102–14114. DOI: 10.1007/s11356-016-6390-1.
Feng, B.W., Li, X.R. & Wang, J.H. (2009). Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. Fems Microbiol. Ecol. 70(2): 80–92. DOI:10.1111/j.1574-6941.2009.00772.x.
Field, C.B. (1998). Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281(5374): 237–240. DOI: 10.1126/science. 281.5374.237.
Flombaum, P., Gallegos, J.L. & Gordillo, R.A. (2013). Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl. Acad. Sci. USA 110(24): 9824–9829. DOI: 10.1073/pnas.1307701110.
Glã Ckner, F.O., Fuchs, B.M. & Amann, R. (1999). Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 65(8): 3721–3726.
Godmaire, H. & Nalewajko, C. (1989). Growth, photosynthesis, and extracellular organic release in colonized. Canadian Journal of Botany 67(12): 3429–3438.
Gordon-Bradley, N., Lymperopoulou, D.S. & Williams, H.N. (2014). Differences in bacterial community structure on Hydrilla verticillata and Vallisneria americana in a freshwater spring. Microbes & Environments 29(1): 67–73. DOI: 10.1264/jsme2.ME13064.
Haller, W.T., Sutton, D.L. & Barlowe, W.C. (1974). Effects of Salinity on Growth of Several Aquatic Macrophytes. Ecology 55(4): 891–894.
He, D., Ren, L. & Wu, Q. (2012). Epiphytic bacterial communities on two common submerged macrophytes in Taihu Lake: diversity and host-specificity. Chinese journal of oceanology and limnology 30(2): 237–247. DOI: 10.1007/s00343-012-1084-0.
He, D., Ren, L. & Wu, Q.L. (2014). Contrasting diversity of epibiotic bacteria and surrounding bacterioplankton of a common submerged macrophyte, Potamogeton crispus, in freshwater lakes. Fems Microbiol. Ecol. 90(3): 551–562. DOI: 10.1111/1574-6941.12414.
Hempel, M., Blume, M. & Blindow, I. (2008). Epiphytic bacterial community composition on two common submerged macrophytes in brackish water and freshwater. Bmc Microbiology 8(1): 58. DOI: 10.1186/1471-2180-8-58.
Hempel, M., Grossart, H.P. & Gross, E.M. (2009). Community composition of bacterial biofilms on two submerged macrophytes and an artificial substrate in a pre-alpine lake. Aquat. Microb. Ecol. 58(1): 79–94. DOI: 10.3354/ame01353.
Huang, J., Xin, Y. & Cao, X. (2011). Phylogenetic diversity and characterization of 2-haloacid degrading bacteria from the marine sponge Hymeniacidon perlevis. World J. Microb. Biot. 27(8): 1787–1794. DOI: 10.1007/s11274-010-0636-8.
Huo, Y.Z., Xu, S.N. & Wang, Y.Y. (2011). Bioremediation efficiencies of gracilaria verrucosa, cultivated in an enclosed sea area of Hangzhou Bay, China. J. Appl. Phycol. 23(2): 173–182. DOI: 10.1007/s10811-010-9584-9.
Huss, A.A. & Wehr, J.D. (2004). Strong Indirect Effects of a Submersed Aquatic Macrophyte, Vallisneria americana, on Bacterioplankton Densities in a Mesotrophic Lake. Microbial Ecol. 47(4): 305–315. DOI: 10.1007/s00248-003-1034-7.
Jiang, R., Wang, J.X. & Huang, B. (2016). Phylogenetic analysis of bacterial community composition in sediments with organic contaminants from the Jiaojiang estuary in China. Mar. Pollut. Bull. 109(1): 558–565. DOI: 10.1016/j.marpolbul.2016.03.046.
Johnson, J.A. & Newman, R.M. (2011). A comparison of two methods for sampling biomass of aquatic plants. J. Aquat. Plant Manage. 49(1): 1–8.
Langille, M.G.I., Zaneveld, J. & Caporaso, J.G. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31(9): 814–821. DOI: 10.1038/nbt.2676.
Li, F., Zhu, L. & Xie, Y. (2016). Fragment growth performance of the invasive submerged macrophyte Myriophyllum spicatum under conditions of different water depths and sediment types. Aquatic Ecology 50(4): 727–734. DOI: 10.1007/s10452-016-9589-9.
Liu, J., Fu, B. & Yang, H. (2015). Phylogenetic shifts of bacterioplankton community composition along the Pearl Estuary: the potential impact of hypoxia and nutrients. Frontiers in Microbiology 6(64): 64. DOI: 10.3389/fmicb.2015.00064.
Liu, Q., Sun, B. & Huo, Y. (2018). Nutrient bioextraction and microalgae growth inhibition using submerged macrophyte Myriophyllum spicatum in a low salinity area of East China Sea. Mar. Pollut. Bull. 127: 67–72. DOI: 10.1016/j.marpolbul.2017.11.031.
Liu, T., Zhang, A.N. & Wang, J. (2018). Integrated biogeography of planktonic and sedimentary bacterial communities in the Yangtze river. Microbiome 6(1): 16. DOI: 10.1186/s40168-017-0388-x.
Lozupone, C.A. & Knight, R. (2007). Global patterns in bacterial diversity. P. Natl Acad. Sci. Usa 104(27): 11436–11440. DOI: 10.1073/pnas.0611525104.
Magoc, T. & Salzberg, S.L. (2011). Flash: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21): 2957–2963. DOI: 10.1093/bioinformatics/btr507.
Markowitz, V.M., Chen, I.A. & Palaniappan, K. (2012). IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res. 40: D115–D122. DOI: 10.1093/nar/gkr1044.
Mcbride, M.J., Liu, W. & Lu, X. (2014). The Family Cytophagaceae. In E. Rosenberg, E. Stackebrandt, F.L. Thompson, S. Lory & E.F. DeLong (Eds.), The Prokaryotes, fourth edn. (pp. 577–593). Springer Berlin Heidelberg, Berlin, Heidelberg. DOI: 10.1007/978-3-642-38954-2_382.
McIlroy, S.J. & Nielsen, P.H. (2014). The family Saprospiraceae. In: Rosenberg, E., Stackebrandt, E., Thompson, F.L., Lory, S. & DeLong, E.F. (Eds.), The Prokaryotes, fourth edn. (pp. 863–889). Berlin, Heidelberg: Springer Berlin Heidelberg. DOI: 10.1007/978-3-642-38954-2_138.
Morozova, O.V., Ratushnyak, A.A. & Yu, O. (2011). The Role of Bacterioplankton and Aquatic Macrophytes in Autopurification of Hydroecosystems Polluted with Phosphorus. Middle-East Journal of Scientific Research 7(3): 346–351.
Novak, H.R., Sayer, C. & Isupov, M.N. (2013). Marine Rhodobacteraceae L-haloacid dehalogenase contains a novel His/Glu dyad that could activate the catalytic water. Febs Journal 280(7): 1664–1680. DOI: 10.1111/febs.12177.
Palenik, B., Brahamsha, B. & Larimer, F.W. (2003). The genome of a motile marine Synechococcus. Nature 424(6952): 1037–1042. DOI: 10.1038/nature01943.
Parfenova, V.V., Gladkikh, A.S. & Belykh, O.I. (2013). Comparative analysis of biodiversity in the planktonic and biofilm bacterial communities in Lake Baikal. Microbiology 82(1): 91–101. DOI: 10.1134/S0026261713010128.
Rimes, C.A. & Goulder, R. (1985). A note on the attachment rate of suspended bacteria to submerged aquatic plants in a calcareous stream. J. Appl. Microbiol. 59(4): 389–392.
Rimes, C.A. & Goulder, R. (1986). Quantitative observations on the ability of epiphytic bacteria to contribute to the populations of suspended bacteria in two dissimilar headstreams. Freshwater Biol. 16(3): 301–311.
Rooney, N. & Kalff, J. (2003). Interactions among epilimnetic phosphorus, phytoplankton biomass and bacterioplankton metabolism in lakes of varying submerged macrophyte cover. Hydrobiologia 501(1–3): 75–81.
Schmalenberger, A., Schwieger, F. & Tebbe, C.C. (2001). Effect of primers hybridizing to different evolutionarily conserved regions of the small-subunit rrna gene in pcr-based microbial community analyses and genetic profiling. Appl. Environ. Microbiol. 67(8): 3557–3563. DOI: 10.1128/AEM.67.8.3557-3563.2001.
Søndergaard, M. (1981). Kinetics of Extracellular Release of 14 C-Labelled Organic Carbon by Submerged Macrophytes. Oikos 36(3): 331–347.
Stanley, N.R. & Lazazzera, B.A. (2004). Environmental signals and regulatory pathways that influence biofilm formation. Mol. Microbiol. 52(4): 917. DOI: 10.1111/j.1365-2958.2004.04036.x.
Van, D.G.K., Vandekerckhove, T. & Vloemans, N. (2005). Characterization of bacterial communities in four freshwater lakes differing in nutrient load and food web structure. Fems Microbiol. Ecol. 53(2): 205–220. DOI: 10.1016/j.femsec.2004.12.006.
Wang, Y., Sheng, H.F. & He, Y. (2012). Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments using millions of Illumina tags. Appl. Environ. Microb. 78(23): 8264–8271. DOI: 10.1128/AEM.01821-12.
Wu, Z., Yu, D. & Wang, Z. (2015). Great influence of geographic isolation on the genetic differentiation of Myriophyllum spicatum under a steep environmental gradient. Scientific Reports 5(4): 15618. DOI: 10.1038/srep15618.
Yang, C., Wang, Q. & Simon, P.N. (2017). Distinct Network Interactions in Particle-Associated and Free-Living Bacterial Communities during a Microcystis aeruginosa Bloom in a Plateau Lake. Front Microbiol 8: 1202. DOI: 10.3389/fmicb.2017.01202.
Zeng, J., Bian, Y. & Xing, P. (2012). Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake. Applied & Environmental Microbiology 78(1): 177–184. DOI: 10.1128/AEM.05117-11.
Zhou, J., Deng, Y. & Luo, F. (2010). Functional molecular ecological networks. mBio 1(4): 1592–1601. DOI: 10.1128/mBio.00169-10.
