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Community Structure and Functional Diversity of Epiphytic Bacteria and Planktonic Bacteria on Submerged Macrophytes in Caohai Lake, Southwest of China

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Community Structure and Functional Diversity of Epiphytic Bacteria and Planktonic Bacteria on Submerged Macrophytes in Caohai Lake, Southwest of China Annals of Microbiology (2019) 69:933–944 https://doi.org/10.1007/s13213-019-01485-4 ORIGINAL ARTICLE Community structure and functional diversity of epiphytic bacteria and planktonic bacteria on submerged macrophytes in Caohai Lake, southwest of China Dingbo Yan1,2 & Pinhua Xia1,2 & Xu Song1,2 & Tao Lin1,2 & Haipeng Cao3 Received: 12 February 2019 /Accepted: 22 May 2019 /Published online: 31 May 2019 # Università degli studi di Milano 2019 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. Keywords Epiphytic bacteria . Planktonic bacteria . Diversity pattern . Functional traits Introduction Electronic supplementary material The online version of this article Epiphytic biofilms are widely distributed on solid surfaces (https://doi.org/10.1007/s13213-019-01485-4) contains supplementary such as rocks, sediments, and submerged plants in ponds, material, which is available to authorized users. rivers, lakes, and marine environments, which harbor a com- bination of algae, protists, fungi, and bacteria (Palmer Jr. and * Pinhua Xia [email protected] White 1997; Writer et al. 2011;Luetal.2016;Zhaoetal. 2018). Biofilms play a major role in regulating the nutrient cycle and energy flow in water bodies, and there is growing 1 Guizhou Province Key Laboratory for Information System of Mountainous Areas and Protection of Ecological Environment, research interest in utilizing natural periphytic biofilms in Guizhou Normal University, Guiyang 550001, China wastewater treatment, nonpoint source pollution control, and 2 Plateau Wetland Ecology and Environment Research Center, remediation of polluted waters (Furey et al. 2016; Singh et al. Guizhou Normal University, Guiyang 550001, China 2017;Suetal.2017;Wuetal.2018). The ecological functions 3 College of Life Sciences, Guizhou Normal University, of biofilms are closely linked to the chelation, recycling, or Guiyang 550001, China metabolic degradation activities of microorganisms on 934 Ann Microbiol (2019) 69:933–944 nutrients and pollutants (Wu et al. 2012;Zhaoetal.2018). microorganisms. It depends on the prokaryotic functional data Therefore, the community structure and ecological functional of culturable bacteria and species classification (OTU table) to characteristics of epiphytic biofilm microorganisms are the obtain community function information, which is applicable hotspots of current water ecology research (Wu et al. 2012; to a variety of environmental samples and has the advantages Wu et al. 2018). Submerged macrophytes are widely distrib- of reliable results and economical and practical benefits uted in shallow water ecosystems, and their leaves provide (Louca et al. 2016; Galand et al. 2018). This provides an epiphytic areas for the growth of microorganisms and have effective solution for understanding the differences in the special niches. However, compared with that of planktonic structure and function of epiphytic and planktonic bacterial bacteria, the understanding of the structure and function of communities. epiphytic bacteria on submerged macrophyte leaves is still This study focuses on the typical macrophytic lake very limited. (Caohai) in southwest China and compares the structure and Some previous studies have shown that distinct and shared function of epiphytic and planktonic bacteria by 16S rRNA microorganisms exist between epiphytic and planktonic bac- gene high-throughput sequencing and functional predictive terial communities (Burke et al. 2011;Heetal.2014). analysis. The study aims to address the following three topics: Planktonic bacteria have been regarded as a major seed bank (i) characteristics of epiphytic and planktonic bacterial com- for epiphytic bacteria, which has an important influence on the munity species composition, (ii) community structure of epi- assemblage of epiphytic bacteria (Dolan 2005; Garulera et al. phytic and planktonic bacteria and their relationship with the 2016). Certainly, host-specific communities can be selected environment, and (iii) epiphytic bacterial community function by complex physical or biochemical characteristics on differ- and its environmental significance. ent plant leaves. Plants and their secretions at different growth stages can also shape the composition of epiphytic bacterial communities (Herrmann et al. 2008; Lachnit et al. 2011;He Material and methods et al. 2012). Environmental factors also have an important impact on epiphytic bacterial communities, such as pH, redox Study site and sampling potential, water flow, light, temperature, and nutrient availability(Bouletreau et al. 2012; Kuehn et al. 2014;Hao The sampling sites were located in the karst area of southwest et al. 2017). For example, the abundances of Actinobacteria, China, Caohai National Nature Reserve (104°1 2′–104° 18′ E, Nitrospirae,andVerrucomicrobia in biofilms vary with the 26° 49′–26° 53′N) with a subtropical semi-humid monsoon conductivity of river water, while the presence of climate. With a water area of 25 km2 and an average temper- Acidobacteria, Gemmatimonadetes,andProteobacteria in ature of 10.5 °C, it is one of the three highest plateau fresh- biofilms is associated with pH changes (Wilhelm et al. 2013; water lakes in China (2171 m above sea level). It is a typical Battin et al. 2016). Similarly, epiphytic bacteria may spread macrophytic lake ecosystem with abundant aquatic vegetation into planktonic bacterial communities (Underwood et al. and a water depth of approximately 3 m. Samples were gath- 2007; Kurian et al. 2012). Clearly, there is a complex interre- ered from 9 sites on the lake in November 2017 (Fig. 1). lationship between epiphytic and planktonic bacteria. Weining County is at the northeast region of the lake, where However, current reports lack the understanding of the simi- a large amount of domestic sewage enters the protected area larities and differences between the structure and function of (S1, S2, S3, and S4, named HP), and has relatively heavy epiphytic and planktonic bacteria. pollution. The southwestern part of the lake has less pollution Species richness or diversity may not be sufficient to un- (S5, S6, S7, S8, and S9, named LP). Submerged macrophytes derstand how community composition and composition affect (Potamogeton lucens) were collected with a hook that was ecosystem function (Loreau et al. 2001; Cardinale et al. 2006). cleared with in situ water. Approximately 10 g of fresh- This shows that in addition to revealing which microorgan- weight leaf samples was cut away from three to five plant isms are in the environment, it is particularly important to replicates and transferred into a sterile 500-mL polyethylene determine the functional profile of microbial communities. bottle containing 400 mL of 50 mM phosphate-buffered saline To this end, researchers have developed a variety of methods (PBS, pH = 7.4) solution for epiphytic bacterial community based on 16S rRNA high-throughput sequencing to predict analysis (Zhang et al. 2016). In addition to plant sampling, bacterial community functions, including the Phylogenetic 1.5-L water samples from the area surrounding the sampling Investigation of Communities by Reconstruction of area for physicochemical and planktonic bacterial community Unobserved States (PICRUSt) (Langille et al. 2013), analysis were collected. All leaf samples were collected in Tax4Fun (Aßhauer et al. 2015), and the Functional three replicates, mixed, kept with ice bags, and quickly Annotation of Prokaryotic Taxa (FAPROTAX) (Louca et al. returned to the laboratory. Dissolved oxygen and pH were 2016). Among them, FAPROTAX is the most commonly used determined using a portable instrument (HQ30d, HACH, method for exploring the biogeochemical cycle functions of USA). The physicochemical
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