Abstract
Purpose
Epiphytic bacteria on the surfaces of submerged macrophytes play an important role in lake biodiversity and ecological processes. However, compared with planktonic bacteria, there is poor understanding of the community structure and function of epiphytic bacteria.
Methods
Here, we used 16S rRNA gene high-throughput sequencing and functional prediction analysis to explore the structural and functional diversity of epiphytic bacteria and planktonic bacteria of a typical submerged macrophyte (Potamogeton lucens) in Caohai Lake.
Results
The results showed that the species composition of epiphytic and planktonic bacteria was highly similar as 88.89% phyla, 77.21% genera and 65.78% OTUs were shared by the two kinds of samples. Proteobacteria and Bacteroidetes were dominant phyla shared by the two kinds of communities. However, there are also some special taxa. Furthermore, the epiphytic bacterial communities exhibited significantly different structures from those in water, and the abundant OTUs had opposite constituents. The explained proportion of the planktonic bacterial community by aquatic environmental parameters is significantly higher than that of epiphytic bacteria, implying that the habitat microenvironment of epiphytic biofilms may be a strong driving force of the epiphytic bacterial community. Functional predictive analysis (Functional Annotation of Prokaryotic Taxa, FAPROTAX) found that epiphytic bacteria and planktonic bacteria are dominated by heterotrophic functions, but epiphytic bacteria have more prominent fermentation and denitrification functions (nitrate reduction, nitrate respiration, and nitrite respiration) than planktonic bacteria.
Conclusion
This study has increased our understanding of the communities and functions of epiphytic bacteria on submerged macrophyte leaves, and their role in lake denitrification cannot be ignored.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Aßhauer KP, Wemheuer B, Daniel R, Meinicke P (2015) Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31(17):2882–2884. https://doi.org/10.1093/bioinformatics/btv287
Battin TJ, Besemer K, Bengtsson MM, Romani AM, Packmann AI (2016) The ecology and biogeochemistry of stream biofilms. Nat Rev Microbiol 14(4):251–263. https://doi.org/10.1038/nrmicro.2016.15
Bengtsson MM, Sjotun K, Lanzen A, Ovreas L (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6(12):2188–2198. https://doi.org/10.1038/ismej.2012.67
Bing H, Zhang SH, Wang PF, Chao W (2018) Effects of water flow on submerged macrophyte-biofilm systems in constructed wetlands. Sci Rep 8(1):2650. https://doi.org/10.1038/s41598-018-21080-y
Bitrian M, González RH, Paris G, Hellingwerf KJ, Nudel CB (2013) Blue-light-dependent inhibition of twitching motility in Acinetobacter baylyi ADP1: additive involvement of three BLUF-domain-containing proteins. Microbiology 159(9):1828–1841. https://doi.org/10.1099/mic.0.069153-0
Bouletreau S, Salvo E, Lyautey E, Mastrorillo S, Garabetian F (2012) Temperature dependence of denitrification in phototrophic river biofilms. Sci Total Environ 416:323–328. https://doi.org/10.1016/j.scitotenv.2011.11.066
Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5(4):590–600. https://doi.org/10.1038/ismej.2010.164
Cao T, Ni L, Xie P (2004) Acute biochemical responses of a submersed macrophyte, Potamogeton crispus L., to high ammonium in an aquarium experiment. J Freshw Ecol 19(2):279–284. https://doi.org/10.1080/02705060.2004.9664542
Cardinale BJ, Srivastava DS, Emmett Duffy J, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443(7114):989–992. https://doi.org/10.1038/nature05202
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42 (Database issue:D633–D642. https://doi.org/10.1093/nar/gkt1244
Dolan JR (2005) An introduction to the biogeography of aquatic microbes. Aquat Microb Ecol 41(1):39–48. https://doi.org/10.3354/ame041039
Filippini M, Buesing N, Gessner MO, Bürgmann H (2009) Microbial communities in contrasting freshwater marsh microhabitats. FEMS Microbiol Ecol 69(1):84–97. https://doi.org/10.1111/j.1574-6941.2009.00692.x
Florez JZ, Camus C, Hengst MB, Buschmann AH (2017) A functional perspective analysis of macroalgae and epiphytic bacterial community interaction. Front Microbiol 8:2561. https://doi.org/10.3389/fmicb.2017.02561
Furey PC, Deininger A, Liess A (2016) Substratum-associated microbiota. Water Environ Res 88(10):1637–1671. https://doi.org/10.2175/106143016x14696400495613
Galand PE, Pereira O, Hochart C, Auguet JC, Debroas D (2018) A strong link between marine microbial community composition and function challenges the idea of functional redundancy. ISME J 12:2470–2478. https://doi.org/10.1038/s41396-018-0158-1
Garulera JB, Vila M, Borrull E, Riobó P, Franco JM, Sala MM (2016) Variability of planktonic and epiphytic vibrios in a coastal environment affected by Ostreopsis blooms. Sci Mar 80S1(S1):97–106. https://doi.org/10.3989/scimar.04405.01A
Hao B, Wu H, Cao Y, Xing W, Jeppesen E, Li W (2017) Comparison of periphyton communities on natural and artificial macrophytes with contrasting morphological structures. Freshw Biol 62(10):1783–1793. https://doi.org/10.1111/fwb.12991
Hassett DJ, Cuppoletti J, Trapnell B, Lymar SV, Rowe JJ, Sun Yoon S, Hilliard GM, Parvatiyar K, Kamani MC, Wozniak DJ, Hwang S-H, McDermott TR, Ochsner UA (2002) Anaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: rethinking antibiotic treatment strategies and drug targets. Adv Drug Deliv Rev 54(11):1425–1443. https://doi.org/10.1016/S0169-409X(02)00152-7
He D, Ren LJ, Wu QL (2012) Epiphytic bacterial communities on two common submerged macrophytes in Taihu Lake: diversity and host-specificity. Chin J Oceanol Limnol 30(2):237–247. https://doi.org/10.1007/s00343-012-1084-0
He D, Ren LJ, Wu QL (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. https://doi.org/10.1111/1574-6941.12414
Herrmann M, Saunders AM, Schramm A (2008) Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl Environ Microbiol 74(10):3279–3283. https://doi.org/10.1128/AEM.02802-07
Hörnström E (2002) Phytoplankton in 63 limed lakes in comparison with the distribution in 500 untreated lakes with varying pH. Hydrobiologia 470(1):115–126. https://doi.org/10.1023/a:1015619921119
Jezberová J, Jezbera J, Brandt U, Lindström ES, Langenheder S, Hahn MW (2010) Ubiquity of Polynucleobacter necessarius ssp. asymbioticus in lentic freshwater habitats of a heterogenous 2000 km2 area. Environ Microbiol 12(3):658–669. https://doi.org/10.1111/j.1462-2920.2009.02106.x
Ji B, Yang K, Zhu L, Jiang Y, Wang HY, Zhou J, Zhang HN (2015) Aerobic denitrification: a review of important advances of the last 30 years. Biotechnol Bioprocess Eng 20(4):643–651. https://doi.org/10.1007/s12257-015-0009-0
Jones SE, McMahon KD (2009) Species-sorting may explain an apparent minimal effect of immigration on freshwater bacterial community dynamics. Environ Microbiol 11(4):905–913. https://doi.org/10.1111/j.1462-2920.2008.01814.x
Kasalický V, Jezbera J, Hahn MW, Šimek K (2013) The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains. PLoS One 8(3):e58209. https://doi.org/10.1371/journal.pone.0058209
Koo H, Strope BM, Kim EH, Shabani AM, Kumar R, Crowley MR, Andersen DT, Bej AK (2016) Draft genome sequence of Janthinobacterium sp. Ant5-2-1, isolated from proglacial Lake Podprudnoye in the Schirmacher oasis of East Antarctica. Genome Announcements 4(1):e01600–e01615. https://doi.org/10.1128/genomeA.01600-15
Kuehn KA, Francoeur SN, Findlay RH, Neely RK (2014) Priming in the microbial landscape: periphytic algal stimulation of litter-associated microbial decomposers. Ecology 95(3):749–762. https://doi.org/10.1890/13-0430.1
Kumar A, Ng DHP, Wu Y, Cao B (2018) Microbial community composition and putative biogeochemical functions in the sediment and water of tropical granite quarry lakes. Microb Ecol 77(1):1–11. https://doi.org/10.1007/s00248-018-1204-2
Kurian PS, Abraham K, Kumar PS (2012) Endophytic bacteria - do they colonize within the plant tissues if applied externally? Curr Sci 103(6):626–628 https://www.jstor.org/stable/24088792
Lachnit T, Meske D, Wahl M, Harder T, Schmitz R (2011) Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13(3):655–665. https://doi.org/10.1111/j.1462-2920.2010.02371.x
Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. https://doi.org/10.1038/nbt.2676
Levi PS, Riis T, Alnøe AB, Peipoch M, Maetzke K, Bruus C, Baattrup-Pedersen A (2015) Macrophyte complexity controls nutrient uptake in lowland streams. Ecosystems 18(5):914–931. https://doi.org/10.1007/s10021-015-9872-y
Liu JZ, Wang FW, Liu W, Tang CL, Wu CX, Wu YH (2016) Nutrient removal by up-scaling a hybrid floating treatment bed (HFTB) using plant and periphyton: from laboratory tank to polluted river. Bioresour Technol 207:142–149. https://doi.org/10.1016/j.biortech.2016.02.011
Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294(5543):804–808. https://doi.org/10.1126/science.1064088
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353(6305):1272–1277. https://doi.org/10.1126/science.aaf4507
Lu HY, Wan JJ, Li JY, Shao HB, Wu YH (2016) Periphytic biofilm: a buffer for phosphorus precipitation and release between sediments and water. Chemosphere 144:2058–2064. https://doi.org/10.1016/j.chemosphere.2015.10.129
Ma Q, Qu YY, Shen WL, Zhang ZJ, Wang JW, Liu ZY, Li DX, Li HJ, Zhou JT (2015) Bacterial community compositions of coking wastewater treatment plants in steel industry revealed by Illumina high-throughput sequencing. Bioresour Technol 179:436. https://doi.org/10.1016/j.biortech.2014.12.041
Matu A, Lum Nde A, Oosthuizen L, Hitzeroth A, Badenhorst M, Duba L, Gidaga M, Klinck J, Kriek I-M, Lekoma PJ, Nel L, dos Ramos SM, Rossouw J, Salomane N, Segone N, Serobe S, Tiyani T, Hugo CJ, Newman JD (2019) Draft genome sequences of seven Chryseobacterium type strains. Microbiology Resource Announcements 8(1):e01518–e01518. https://doi.org/10.1128/mra.01518-18
Madigan MT, Martinko JM, Stahl DA, Clark DP (2005) Brock biology of microorganisms (11th ed.) Benjamin Cummings: Boston
Mori H, Maruyama F, Kato H, Toyoda A, Dozono A, Ohtsubo Y, Nagata Y, Fujiyama A, Tsuda M, Kurokawa K (2013) Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes. DNA Res 21(2):217–227. https://doi.org/10.1093/dnares/dst052
Ordoñez OF, Lanzarotti E, Kurth D, Gorriti MF, Revale S, Cortez N, Vazquez MP, Farías ME, Turjanski AG (2013) Draft genome sequence of the polyextremophilic Exiguobacterium sp. strain S17, isolated from hyperarsenic lakes in the Argentinian Puna. Genome announcements 1(4):e00480–e00413. https://doi.org/10.1128/genomeA.00480-13
Palmer RJ Jr, White DC (1997) Developmental biology of biofilms: implications for treatment and control. Trends Microbiol 5(11):435–440. https://doi.org/10.1016/S0966-842X(97)01142-6
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30(21):3123–3124. https://doi.org/10.1093/bioinformatics/btu494
Patel V, Munot H, Shouche YS, Madamwar D (2014) Response of bacterial community structure to seasonal fluctuation and anthropogenic pollution on coastal water of Alang-Sosiya ship breaking yard, Bhavnagar, India. Bioresour Technol 161:362–370. https://doi.org/10.1016/j.biortech.2014.03.033
Paul C, Pohnert G (2011) Production and role of volatile halogenated compounds from marine algae. Cheminform 42(21):186. https://doi.org/10.1002/chin.201121253
Sandjensen K, Revsbech NP, Jørgensen BB (1985) Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Mar Biol 89(1):55–62. https://doi.org/10.1007/BF00392877
Seymour JR, Amin SA, Raina JB, Stocker R (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2:17065. https://doi.org/10.1038/nmicrobiol.2017.65
Singh S, James A, Bharose R (2017) Biological assessment of water pollution using periphyton productivity: a review. Nat Environ Pollut Technol 16(2):559–567
Song YZ, Wang JQ, Gao YX, Xie XJ (2015) The physiological responses of Vallisneria natans to epiphytic algae with the increase of N and P concentrations in water bodies. Environ Sci Pollut Res 22(11):8480–8487. https://doi.org/10.1007/s11356-014-3998-x
Su J, Kang D, Xiang W, Wu CX (2017) Periphyton biofilm development and its role in nutrient cycling in paddy microcosms. J Soils Sediments:810–819. https://doi.org/10.1007/s11368-016-1575-2
Underwood W, Melotto M, He S (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9(7):1621–1629. https://doi.org/10.1111/j.1462-5822.2007.00938.x
Wei Z, Liu Y, Feng K, Li S, Wang S, Jin D, Zhang Y, Chen H, Yin H, Xu M, Deng Y (2018) The divergence between fungal and bacterial communities in seasonal and spatial variations of wastewater treatment plants. Sci Total Environ 628-629(1):969–978. https://doi.org/10.1016/j.scitotenv.2018.02.003
Wilhelm L, Singer GA, Fasching C, Battin TJ, Besemer K (2013) Microbial biodiversity in glacier-fed streams. ISME J 7(8):1651–1660. https://doi.org/10.1038/ismej.2013.44
Writer JH, Ryan JN, Barber LB (2011) Role of biofilms in sorptive removal of steroidal hormones and 4-nonylphenol compounds from streams. Environ Sci Technol 45(17):7275–7283. https://doi.org/10.1021/es2008038
Wu YH, Li TL, Yang LZ (2012) Mechanisms of removing pollutants from aqueous solutions by microorganisms and their aggregates: a review. Bioresour Technol 107:10–18. https://doi.org/10.1016/j.biortech.2011.12.088
Wu YH, Liu JZ, Rene ER (2018) Periphytic biofilms: a promising nutrient utilization regulator in wetlands. Bioresour Technol 248:44–48. https://doi.org/10.1016/j.biortech.2017.07.081
Xie WY, Su JQ, Zhu YG (2015) Phyllosphere bacterial community of floating macrophytes in paddy soil environments as revealed by illumina high-throughput sequencing. Appl Environ Microbiol 81(2):522–532. https://doi.org/10.1128/aem.03191-14
Xu N, Tan G, Wang H, Gai X (2016) Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol 74:1–8. https://doi.org/10.1016/j.ejsobi.2016.02.004
Yan LY, Zhang SH, Lin D, Guo C, Yan LL, Wang SP, He ZL (2018) Nitrogen loading affects microbes, nitrifiers and denitrifiers attached to submerged macrophyte in constructed wetlands. Sci Total Environ 622-623:121–126. https://doi.org/10.1016/j.scitotenv.2017.11.234
Yan L, Mu X, Han B, Zhang S, Qiu C, Ohore OE (2019) Ammonium loading disturbed the microbial food webs in biofilms attached to submersed macrophyte Vallisneria natans. Sci Total Environ 659:691–698. https://doi.org/10.1016/j.scitotenv.2018.12.423
Zhang SH, Pang S, Wang PF, Wang C, Guo C, Addo FG, Li Y (2016) Responses of bacterial community structure and denitrifying bacteria in biofilm to submerged macrophytes and nitrate. Sci Rep 6:36178. https://doi.org/10.1038/srep36178
Zhao YH, Xiong X, Wu CX, Xia YQ, Li JY, Wu YH (2018) Influence of light and temperature on the development and denitrification potential of periphytic biofilms. Sci Total Environ 613-614:1430–1437. https://doi.org/10.1016/j.scitotenv.2017.06.117
Funding
This project was financially supported by the National Natural Science Foundation of China (41867056), Major Project of Guizhou Province (20163022), Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province (U1812401), and Guizhou Science and Technology Plan Project (20185769).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies performed by any of the authors with human participants.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 415 kb)
Rights and permissions
About this article
Cite this article
Yan, D., Xia, P., Song, X. et al. Community structure and functional diversity of epiphytic bacteria and planktonic bacteria on submerged macrophytes in Caohai Lake, southwest of China. Ann Microbiol 69, 933–944 (2019). https://doi.org/10.1007/s13213-019-01485-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-019-01485-4