Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom

Cyanobacterial harmful algal blooms (cyanoHABs) appear to be increasing in frequency on a global scale. The Cyanobacteria in blooms can produce toxic secondary metabolites that make freshwater dangerous for drinking and recreation. To characterize microbial activities in a cyanoHAB, transcripts from...

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Main Authors: Penn, Kevin, Wang, Jia, Fernando, Samodha C., Thompson, Janelle Renee
Other Authors: Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Format: Article
Language:en_US
Published: Nature Publishing Group/nternational Society for Microbial Ecology 2014
Online Access:http://hdl.handle.net/1721.1/89638
https://orcid.org/0000-0002-1123-8458
https://orcid.org/0000-0001-8667-8186
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author Penn, Kevin
Wang, Jia
Fernando, Samodha C.
Thompson, Janelle Renee
author2 Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
author_facet Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Penn, Kevin
Wang, Jia
Fernando, Samodha C.
Thompson, Janelle Renee
author_sort Penn, Kevin
collection MIT
description Cyanobacterial harmful algal blooms (cyanoHABs) appear to be increasing in frequency on a global scale. The Cyanobacteria in blooms can produce toxic secondary metabolites that make freshwater dangerous for drinking and recreation. To characterize microbial activities in a cyanoHAB, transcripts from a eutrophic freshwater reservoir in Singapore were sequenced for six samples collected over one day-night period. Transcripts from the Cyanobacterium Microcystis dominated all samples and were accompanied by at least 533 genera primarily from the Cyanobacteria, Proteobacteria, Bacteroidetes and Actinobacteria. Within the Microcystis population, abundant transcripts were from genes for buoyancy, photosynthesis and synthesis of the toxin microviridin, suggesting that these are necessary for competitive dominance in the Reservoir. During the day, Microcystis transcripts were enriched in photosynthesis and energy metabolism while at night enriched pathways included DNA replication and repair and toxin biosynthesis. Microcystis was the dominant source of transcripts from polyketide and non-ribosomal peptide synthase (PKS and NRPS, respectively) gene clusters. Unexpectedly, expression of all PKS/NRPS gene clusters, including for the toxins microcystin and aeruginosin, occurred throughout the day-night cycle. The most highly expressed PKS/NRPS gene cluster from Microcystis is not associated with any known product. The four most abundant phyla in the reservoir were enriched in different functions, including photosynthesis (Cyanobacteria), breakdown of complex organic molecules (Proteobacteria), glycan metabolism (Bacteroidetes) and breakdown of plant carbohydrates, such as cellobiose (Actinobacteria). These results provide the first estimate of secondary metabolite gene expression, functional partitioning and functional interplay in a freshwater cyanoHAB.
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spelling mit-1721.1/896382022-09-30T23:06:28Z Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom Penn, Kevin Wang, Jia Fernando, Samodha C. Thompson, Janelle Renee Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Penn, Kevin Wang, Jia Fernando, Samodha C. Thompson, Janelle Renee Cyanobacterial harmful algal blooms (cyanoHABs) appear to be increasing in frequency on a global scale. The Cyanobacteria in blooms can produce toxic secondary metabolites that make freshwater dangerous for drinking and recreation. To characterize microbial activities in a cyanoHAB, transcripts from a eutrophic freshwater reservoir in Singapore were sequenced for six samples collected over one day-night period. Transcripts from the Cyanobacterium Microcystis dominated all samples and were accompanied by at least 533 genera primarily from the Cyanobacteria, Proteobacteria, Bacteroidetes and Actinobacteria. Within the Microcystis population, abundant transcripts were from genes for buoyancy, photosynthesis and synthesis of the toxin microviridin, suggesting that these are necessary for competitive dominance in the Reservoir. During the day, Microcystis transcripts were enriched in photosynthesis and energy metabolism while at night enriched pathways included DNA replication and repair and toxin biosynthesis. Microcystis was the dominant source of transcripts from polyketide and non-ribosomal peptide synthase (PKS and NRPS, respectively) gene clusters. Unexpectedly, expression of all PKS/NRPS gene clusters, including for the toxins microcystin and aeruginosin, occurred throughout the day-night cycle. The most highly expressed PKS/NRPS gene cluster from Microcystis is not associated with any known product. The four most abundant phyla in the reservoir were enriched in different functions, including photosynthesis (Cyanobacteria), breakdown of complex organic molecules (Proteobacteria), glycan metabolism (Bacteroidetes) and breakdown of plant carbohydrates, such as cellobiose (Actinobacteria). These results provide the first estimate of secondary metabolite gene expression, functional partitioning and functional interplay in a freshwater cyanoHAB. Singapore. National Research Foundation (Singapore MIT Alliance for Research and Technology (SMART), Center for Environmental Sensing and Modeling (CENSAM) research program) National Science Foundation (U.S.) (Postdoctoral Research Fellowship in Biology, Grant No. DBI-1202865) National Institute of Environmental Health Sciences (NIEHS Grant P30-ES002109 to the MIT Center for Environmental Health Sciences) MIT International Science and Technology Initiatives (MISTI-Hayashi fund) 2014-09-15T20:27:56Z 2014-09-15T20:27:56Z 2014-03 2014-01 Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 http://hdl.handle.net/1721.1/89638 Penn, Kevin, Jia Wang, Samodha C Fernando, and Janelle R Thompson. “Secondary Metabolite Gene Expression and Interplay of Bacterial Functions in a Tropical Freshwater Cyanobacterial Bloom.” ISME J 8, no. 9 (March 20, 2014): 1866–1878. https://orcid.org/0000-0002-1123-8458 https://orcid.org/0000-0001-8667-8186 en_US http://dx.doi.org/10.1038/ismej.2014.27 ISME Journal Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License http://creativecommons.org/licenses/by-nc-sa/3.0/ application/pdf Nature Publishing Group/nternational Society for Microbial Ecology ISME Journal
spellingShingle Penn, Kevin
Wang, Jia
Fernando, Samodha C.
Thompson, Janelle Renee
Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom
title Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom
title_full Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom
title_fullStr Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom
title_full_unstemmed Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom
title_short Secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom
title_sort secondary metabolite gene expression and interplay of bacterial functions in a tropical freshwater cyanobacterial bloom
url http://hdl.handle.net/1721.1/89638
https://orcid.org/0000-0002-1123-8458
https://orcid.org/0000-0001-8667-8186
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