Metagenomic insights into the effects of submerged plants on functional potential of microbial communities in wetland sediments

Fanshu Xiao,Binhao Wang,Zhili He,Huang Yu,Xueqin Yang,Qingyun Yan,Ruiwen Hu,Xiaoli Yu,Yingli Lian,Hangjun Zhang,Xiafei Zheng

doi:10.1007/s42995-021-00100-3

Abstract

Submerged plants in wetlands play important roles as ecosystem engineers to improve self-purification and promote elemental cycling. However, their effects on the functional capacity of microbial communities in wetland sediments remain poorly understood. Here, we provide detailed metagenomic insights into the biogeochemical potential of microbial communities in wetland sediments with and without submerged plants (i.e., Vallisneria natans). A large number of functional genes involved in carbon (C), nitrogen (N) and sulfur (S) cycling were detected in the wetland sediments. However, most functional genes showed higher abundance in sediments with submerged plants than in those without plants. Based on the comparison of annotated functional genes in the N and S cycling databases (i.e., NCycDB and SCycDB), we found that genes involved in nitrogen fixation (e.g., nifD/H/K/W), assimilatory nitrate reduction (e.g., nasA and nirA), denitrification (e.g., nirK/S and nosZ), assimilatory sulfate reduction (e.g., cysD/H/J/N/Q and sir), and sulfur oxidation (e.g., glpE, soeA, sqr and sseA) were significantly higher (corrected p < 0.05) in vegetated vs. unvegetated sediments. This could be mainly driven by environmental factors including total phosphorus, total nitrogen, and C:N ratio. The binning of metagenomes further revealed that some archaeal taxa could have the potential of methane metabolism including hydrogenotrophic, acetoclastic, and methylotrophic methanogenesis, which are crucial to the wetland methane budget and carbon cycling. This study opens a new avenue for linking submerged plants with microbial functions, and has further implications for understanding global carbon, nitrogen and sulfur cycling in wetland ecosystems.

Highlights

Wetlands play important roles in global carbon (C), nitrogen (N) and sulfur (S) cycling, and contribute significantly to the processes of methane production (Borrel et al 2011; Emilson et al 2018), nitrogen transformation and removal (Harrison et al 2009; Liu et al 2018), and sulfur reduction and oxidation (Holmer and Storkholm 2001; Purcell et al 2014)
In this study, detailed metagenomic analyses of microbial genes involved in the nitrogen cycle, sulfur cycle and methanogenesis affected by V. natans in urban wetlands of the Xixi National Wetland Park were performed
Our results showed that V. natans increased the relative abundances of most functional genes involved in the transformation of carbon, nitrogen and sulfur in the wetland sediments

Summary

Introduction

Wetlands play important roles in global carbon (C), nitrogen (N) and sulfur (S) cycling, and contribute significantly to the processes of methane production (Borrel et al 2011; Emilson et al 2018), nitrogen transformation and removal (Harrison et al 2009; Liu et al 2018), and sulfur reduction and oxidation (Holmer and Storkholm 2001; Purcell et al 2014). Aquatic macrophytes (e.g., Vallisneria natans, Hydrilla verticillata and Typha latifolia) are commonly used as biological tools for reducing nitrogen and sulfur elements, and raising dissolved oxygen (DO) concentration in natural or constructed wetlands (Chen et al 2014; Qiu et al 2001; Zhu et al 2016). They almost invariably show positive effects on improving water clarity and increasing the stability of aquatic ecosystems by a variety of different mechanisms (Scheffer et al 1993; Zhu et al 2016). Plants may regulate rhizosphere microorganisms to improve their own fitness (Zhalnina et al 2018)

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