Abstract

Freshwater lakes are threatened by harmful cyanobacterial blooms, whose basic unit is Cyanobacterial Aggregate (CA). CA-attached bacteria play a significant role through different blooming stages with substantial variation of their taxonomic structure. However, little is known about their functional variations and functional links with cyanobacteria due to the lack of reference genomes. In this longitudinal study, we collected 16 CA samples from Lake Taihu, one of China's largest freshwater lakes, from April 2015 to February 2016, and sequenced their V4 region of 16S rRNA genes, full metagenomes (MG), and metatranscriptomes (MT). The analysis of these data revealed the dynamics of microbial taxonomic and functional structure in CAs, influenced by both external environmental factors and internal metabolism. 55 OTUs, 456 genes, and 37 transcripts showed significantly differential abundance across the early, middle, and late blooming stages (ANOVA test, P < 0.05). Total nitrogen and total phosphorus were proved to be the most important environmental drivers of microbial taxonomic and functional variations in CAs (Mantel's r > 0.25, P < 0.05). We constructed 161 high-quality metagenome-assembled genomes (MAGs), out of which 22 were cyanobacterial strains with diverse energy pathways, transporters and prokaryotic defense systems. Based on these MAGs, we constructed a cyanobacteria-bacteria co-nitrogen-pathway and a cyanobacteria-bacteria co-phosphorus-pathway, by which we demonstrated how nitrogen and phosphorus influence the dynamics of the microbial structure to a certain extent by affecting these co-pathways. Overall, these results characterized the taxonomic, functional, and transcriptional variations of microbes in CAs through different blooming stages. Genome assembly and metabolic analysis of cyanobacteria and their attached bacteria suggested that the material exchange and signal transduction do, indeed, exist among them. Our understanding of the underlying molecular pathways for cyanobacterial blooms could lead to the control of blooms by interventional strategies to disrupt critical microbes' expression.

Highlights

  • Eutrophication has threatened freshwater lakes worldwide, leading to Cyanobacterial Harmful Algal Blooms (CyanoHABs) [1, 2]

  • 55 Operational Taxonomic Units (OTUs), 456 genes and 37 transcripts mainly associated with pathways of transporters, photosystem and energy metabolism showed significantly different abundance among the three stages

  • Our understanding of the underlying molecular pathways for cyanobacterial blooms could potentially lead to the control of blooms by interventional strategies to disrupt the expression of critical microbes

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Summary

Introduction

Eutrophication has threatened freshwater lakes worldwide, leading to Cyanobacterial Harmful Algal Blooms (CyanoHABs) [1, 2]. Alternate succession of two cyanobacteria genera (Microcystis and Dolichospermum) was found and the attached bacteria in CA changed along the cyanobacterial succession along different blooming stages [10]. It is unknown whether the genes and transcripts expressed by these bacteria will change significantly at different stages. Mutualistic relationships between cyanobacteria and many attached bacteria have been proposed [11,12,13,14] It failed to explain the phenomenon from the perspective of microbe genes and transcripts, because of the lack of reference genome which are critical for uncovering the cellular and molecular mechanisms. Most bacterial genomes in CA were not constructed in existing database, which limits our understanding of the bacterial variations as responses to cyanobacterial blooms

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