Microbial diversity, genomics, and phage–host interactions of cyanobacterial harmful algal blooms

Author:

Krausfeldt Lauren E.1ORCID,Shmakova Elizaveta1,Lee Hyo Won1,Mazzei Viviana2ORCID,Loftin Keith A.3ORCID,Smith Robert P.14ORCID,Karwacki Emily2,Fortman P. Eric1,Rosen Barry H.5ORCID,Urakawa Hidetoshi5ORCID,Dadlani Manoj6ORCID,Colwell Rita R.7ORCID,Lopez Jose V.1ORCID

Affiliation:

1. Department of Biological Sciences, Guy Harvey Oceanographic Center, Nova Southeastern University, Dania Beach, Florida, USA

2. U.S. Geological Survey, Caribbean–Florida Water Science Center, Orlando, Florida, USA

3. U.S. Geological Survey, Kansas Water Science Center, Lawrence, Kansas, USA

4. Cell Therapy Institute, Kiran Patel College of Allopathic Medicine, Nova Southeastern University, Fort Lauderdale, Florida, USA

5. Department of Ecology and Environmental Studies, Florida Gulf Coast University, Fort Myers, Florida, USA

6. CosmosID, Rockville, Maryland, USA

7. Institute for Advanced Computer Studies, University of Maryland College Park, College Park, Maryland, USA

Abstract

ABSTRACT The occurrence of cyanobacterial harmful algal blooms (cyanoHABs) is related to their physical and chemical environment. However, less is known about their associated microbial interactions and processes. In this study, cyanoHABs were analyzed as a microbial ecosystem, using 1 year of 16S rRNA sequencing and 70 metagenomes collected during the bloom season from Lake Okeechobee (Florida, USA). Biogeographical patterns observed in microbial community composition and function reflected ecological zones distinct in their physical and chemical parameters that resulted in bloom “hotspots” near major lake inflows. Changes in relative abundances of taxa within multiple phyla followed increasing bloom severity. Functional pathways that correlated with increasing bloom severity encoded organic nitrogen and phosphorus utilization, storage of nutrients, exchange of genetic material, phage defense, and protection against oxidative stress, suggesting that microbial interactions may promote cyanoHAB resilience. Cyanobacterial communities were highly diverse, with picocyanobacteria ubiquitous and oftentimes most abundant, especially in the absence of blooms. The identification of novel bloom-forming cyanobacteria and genomic comparisons indicated a functionally diverse cyanobacterial community with differences in its capability to store nitrogen using cyanophycin and to defend against phage using CRISPR and restriction-modification systems. Considering blooms in the context of a microbial ecosystem and their interactions in nature, physiologies and interactions supporting the proliferation and stability of cyanoHABs are proposed, including a role for phage infection of picocyanobacteria. This study displayed the power of “-omics” to reveal important biological processes that could support the effective management and prediction of cyanoHABs. IMPORTANCE Cyanobacterial harmful algal blooms pose a significant threat to aquatic ecosystems and human health. Although physical and chemical conditions in aquatic systems that facilitate bloom development are well studied, there are fundamental gaps in the biological understanding of the microbial ecosystem that makes a cyanobacterial bloom. High-throughput sequencing was used to determine the drivers of cyanobacteria blooms in nature. Multiple functions and interactions important to consider in cyanobacterial bloom ecology were identified. The microbial biodiversity of blooms revealed microbial functions, genomic characteristics, and interactions between cyanobacterial populations that could be involved in bloom stability and more coherently define cyanobacteria blooms. Our results highlight the importance of considering cyanobacterial blooms as a microbial ecosystem to predict, prevent, and mitigate them.

Funder

DOD | USA | U.S. Army Corps of Engineers

USGS Environmental Health Program

Publisher

American Society for Microbiology

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