Depth-dependent variability of biological nitrogen fixation and diazotrophic communities in mangrove sediments

Zhiwen Luo,Qingyun Yan,Xingyu Liu,Wenjun Xu,Yongjie Wu,Qiuping Zhong,Weiming Huang,Wei Zhuang,Cheng Wang,Xingguo Han,Zhengyuan Zhou,Zhili He,Ruiwen Hu

doi:10.1186/s40168-021-01164-0

Abstract

BackgroundNitrogen-fixing prokaryotes (diazotrophs) contribute substantially to nitrogen input in mangrove sediments, and their structure and nitrogen fixation rate (NFR) are significantly controlled by environmental conditions. Despite the well-known studies on diazotrophs in surficial sediments, the diversity, structure, and ecological functions of diazotrophic communities along environmental gradients of mangrove sediment across different depths are largely unknown. Here, we investigated how biological nitrogen fixation varied with the depth of mangrove sediments from the perspectives of both NFR and diazotrophic communities.ResultsThrough acetylene reduction assay, nifH gene amplicon and metagenomic sequencing, we found that the NFR increased but the diversity of diazotrophic communities decreased with the depth of mangrove sediments. The structure of diazotrophic communities at different depths was largely driven by salinity and exhibited a clear divergence at the partitioning depth of 50 cm. Among diazotrophic genera correlated with NFR, Agrobacterium and Azotobacter were specifically enriched at 50–100 cm sediments, while Anaeromyxobacter, Rubrivivax, Methylocystis, Dickeya, and Methylomonas were more abundant at 0–50 cm. Consistent with the higher NFR, metagenomic analysis demonstrated the elevated abundance of nitrogen fixation genes (nifH/D/K) in deep sediments, where nitrification genes (amoA/B/C) and denitrification genes (nirK and norB) became less abundant. Three metagenome-assembled genomes (MAGs) of diazotrophs from deep mangrove sediments indicated their facultatively anaerobic and mixotrophic lifestyles as they contained genes for low-oxygen-dependent metabolism, hydrogenotrophic respiration, carbon fixation, and pyruvate fermentation.ConclusionsThis study demonstrates the depth-dependent variability of biological nitrogen fixation in terms of NFR and diazotrophic communities, which to a certain extent relieves the degree of nitrogen limitation in deep mangrove sediments.BxKuS27-gQH4xs4TJqgBb7Video

Highlights

Nitrogen-fixing prokaryotes contribute substantially to nitrogen input in mangrove sediments, and their structure and nitrogen fixation rate (NFR) are significantly controlled by environmental conditions
Such knowledge was almost inferred from taxonomic information of diazotrophic communities via either 16S Ribosomal RNA (rRNA) or nifH gene amplicon sequencing, and a robust evidence for the activity, diversity, and versatile functions of diazotrophs is still missing in mangrove ecosystems
We investigated the in-depth profile of biological nitrogen fixation and its downstream processes of nitrogen cycling in mangrove sediments, which is crucial for our better understanding of the prevalent nitrogen limitation across wetlands

Summary

Introduction

Nitrogen-fixing prokaryotes (diazotrophs) contribute substantially to nitrogen input in mangrove sediments, and their structure and nitrogen fixation rate (NFR) are significantly controlled by environmental conditions. Some sulfate-reducing bacteria (i.e., Desulfobacteraceae, Desulfovibrionaceae, and Desulfuromonadaceae) were identified as diazotrophs in mangrove sediments, which indicated their potential roles in the cycling of multiple elements [11, 13]. Such knowledge was almost inferred from taxonomic information of diazotrophic communities via either 16S rRNA or nifH gene amplicon sequencing, and a robust evidence for the activity, diversity, and versatile functions of diazotrophs is still missing in mangrove ecosystems

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