Comparative Metagenomics of Toxic Freshwater Cyanobacteria Bloom Communities on Two Continents

Morgan M Steffen,Loren J Hauser,Gregory L Boyer,Steven W Wilhelm,Zhou Li,T Chad Effler,Stefan Bertilsson

doi:10.1371/journal.pone.0044002

Abstract

Toxic cyanobacterial blooms have persisted in freshwater systems around the world for centuries and appear to be globally increasing in frequency and severity. Toxins produced by bloom-associated cyanobacteria can have drastic impacts on the ecosystem and surrounding communities, and bloom biomass can disrupt aquatic food webs and act as a driver for hypoxia. Little is currently known regarding the genomic content of the Microcystis strains that form blooms or the companion heterotrophic community associated with bloom events. To address these issues, we examined the bloom-associated microbial communities in single samples from Lake Erie (North America), Lake Tai (Taihu, China), and Grand Lakes St. Marys (OH, USA) using comparative metagenomics. Together the Cyanobacteria and Proteobacteria comprised >90% of each bloom bacterial community sample, although the dominant phylum varied between systems. Relative to the existing Microcystis aeruginosa NIES 843 genome, sequences from Lake Erie and Taihu revealed a number of metagenomic islands that were absent in the environmental samples. Moreover, despite variation in the phylogenetic assignments of bloom-associated organisms, the functional potential of bloom members remained relatively constant between systems. This pattern was particularly noticeable in the genomic contribution of nitrogen assimilation genes. In Taihu, the genetic elements associated with the assimilation and metabolism of nitrogen were predominantly associated with Proteobacteria, while these functions in the North American lakes were primarily contributed to by the Cyanobacteria. Our observations build on an emerging body of metagenomic surveys describing the functional potential of microbial communities as more highly conserved than that of their phylogenetic makeup within natural systems.

Highlights

The theory that microbial community structure dictates the function of that community has recently been called into question [1,2]
Sequences from each metagenome assigned a best hit identity of Microcystis were aligned to the Microcystis aeruginosa NIES 843 genome [41]
Robust recruitment, covering of 79% of the NIES 843 reference genome, resulted from alignment of Lake Erie sequences, with 92% of the 5539 Microcystis sequences recruited to the NIES 843 scaffold repeated at least once in the Erie metagenome (Figure 1C)

Summary

Introduction

The theory that microbial community structure dictates the function of that community has recently been called into question [1,2]. A shift to whole community shotgun metagenomics has, allowed for a more comprehensive examination of microbial functional genes present in a wealth of natural environments. This technique circumvents the need for culture-based analysis and is more representative of natural community structure and functional potential. One environment of particular concern is the freshwater systems that have in recent years been increasingly inundated by toxic cyanobacterial blooms. These blooms have been responsible for the deterioration of freshwater systems with increasing frequency and intensity and are commonly dominated by colonial cyanobacteria of the genus Microcystis [6,7,8]. Microcystis aeruginosa is commonly dominant within freshwater blooms and has been shown to impact local ecology by disruption of the food web and induction of hypoxia in large lake systems [13,14]

Methods

Results

Conclusion