Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)

Emily J. Davenport; Michelle J. Neudeck; Paul G. Matson; George S. Bullerjahn; Timothy W. Davis; Steven W. Wilhelm; Maddie K. Denney; Lauren E. Krausfeldt; Joshua M.A. Stough; Kevin A. Meyer; Gregory J. Dick; Thomas H. Johengen; Erika Lindquist; Susannah G. Tringe; Robert Michael L. McKay

doi:10.3389/fmicb.2019.02081

Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)

Emily J. Davenport, Michelle J. Neudeck, Paul G. Matson, George S. Bullerjahn, Timothy W. Davis, Steven W. Wilhelm, Maddie K. Denney, Lauren E. Krausfeldt, Joshua M.A. Stough, Kevin A. Meyer, Gregory J. Dick, Thomas H. Johengen, Erika Lindquist, Susannah G. Tringe, Robert Michael L. McKay

Research output: Contribution to journal › Article › peer-review

23 Scopus citations

Abstract

This study examined diel shifts in metabolic functions of Microcystis spp. during a 48-h Lagrangian survey of a toxin-producing cyanobacterial bloom in western Lake Erie in the aftermath of the 2014 Toledo Water Crisis. Transcripts mapped to the genomes of recently sequenced lower Great Lakes Microcystis isolates showed distinct patterns of gene expression between samples collected across day (10:00 h, 16:00 h) and night (22:00 h, 04:00 h). Daytime transcripts were enriched in functions related to Photosystem II (e.g., psbA), nitrogen and phosphate acquisition, cell division (ftsHZ), heat shock response (dnaK, groEL), and uptake of inorganic carbon (rbc, bicA). Genes transcribed during nighttime included those involved in phycobilisome protein synthesis and Photosystem I core subunits. Hierarchical clustering and principal component analysis (PCA) showed a tightly clustered group of nighttime expressed genes, whereas daytime transcripts were separated from each other over the 48-h duration. Lack of uniform clustering within the daytime transcripts suggested that the partitioning of gene expression in Microcystis is dependent on both circadian regulation and physicochemical changes within the environment.

Original language	English
Article number	2081
Journal	Frontiers in Microbiology
Volume	10
DOIs	https://doi.org/10.3389/fmicb.2019.02081
State	Published - Sep 10 2019
Externally published	Yes

Funding

We thank Taylor Tuttle for assistance with sampling. We thank the captain and crew of the NOAA Great Lakes Environmental Research Laboratory for the research vessel used in this study. We would also like to thank Sunit Jain (Second Genome, South San Francisco, CA, United States) for initial quality control and assembly of Microcystis genomes, and Paul Den Uyl for extracting DNAs from Microcystis cultures for sequencing. Funding. GB was supported by NOAA’s Ohio Sea Grant College Program, R/ER-104 (jointly with RMLM) and by funding from the NIH (1P01ES028939-01) and NSF (OCE-1840715) to the Great Lakes Center for Fresh Waters and Human Health, Bowling Green State University. SW was supported by the National Science Foundation (IOS-1451528). The work conducted by the U.S. DOE Joint Genome Institute, a DOE Office of Science User Facility, was supported by the Office of Science of the U.S. DOE under Contract No. DE-AC02-05CH11231. GD and KM were supported by grants from the University of Michigan Office for Research MCubed program and the Erb Family Foundation made through the University of Michigan Water Center. Additional funding was provided to the Cooperative Institute for Great Lakes Research (CIGLR) through the NOAA Cooperative Agreement with University of Michigan (NA17OAR4320152). This is CIGLR contribution number 1147.

Funders	Funder number
Cooperative Institute for Great Lakes Research	1147, NA17OAR4320152
RMLM
National Science Foundation	1451528, IOS-1451528, OCE-1840715, 1840715
National Institutes of Health	1P01ES028939-01
U.S. Department of Energy	DE-AC02-05CH11231
National Oceanic and Atmospheric Administration
Ohio Sea Grant College, Ohio State University
Office of Science
Bowling Green State University
University of Michigan
Boler Family Foundation
Joint Genome Institute
U-M Water Center

Keywords

Lake Erie
Microcystis
cyanobacterial blooms
metatranscriptomics
microcystin

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10.3389/fmicb.2019.02081

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Davenport, E. J., Neudeck, M. J., Matson, P. G., Bullerjahn, G. S., Davis, T. W., Wilhelm, S. W., Denney, M. K., Krausfeldt, L. E., Stough, J. M. A., Meyer, K. A., Dick, G. J., Johengen, T. H., Lindquist, E., Tringe, S. G., & McKay, R. M. L. (2019). Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States). Frontiers in Microbiology, 10, Article 2081. https://doi.org/10.3389/fmicb.2019.02081

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title = "Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)",

abstract = "This study examined diel shifts in metabolic functions of Microcystis spp. during a 48-h Lagrangian survey of a toxin-producing cyanobacterial bloom in western Lake Erie in the aftermath of the 2014 Toledo Water Crisis. Transcripts mapped to the genomes of recently sequenced lower Great Lakes Microcystis isolates showed distinct patterns of gene expression between samples collected across day (10:00 h, 16:00 h) and night (22:00 h, 04:00 h). Daytime transcripts were enriched in functions related to Photosystem II (e.g., psbA), nitrogen and phosphate acquisition, cell division (ftsHZ), heat shock response (dnaK, groEL), and uptake of inorganic carbon (rbc, bicA). Genes transcribed during nighttime included those involved in phycobilisome protein synthesis and Photosystem I core subunits. Hierarchical clustering and principal component analysis (PCA) showed a tightly clustered group of nighttime expressed genes, whereas daytime transcripts were separated from each other over the 48-h duration. Lack of uniform clustering within the daytime transcripts suggested that the partitioning of gene expression in Microcystis is dependent on both circadian regulation and physicochemical changes within the environment.",

keywords = "Lake Erie, Microcystis, cyanobacterial blooms, metatranscriptomics, microcystin",

author = "Davenport, {Emily J.} and Neudeck, {Michelle J.} and Matson, {Paul G.} and Bullerjahn, {George S.} and Davis, {Timothy W.} and Wilhelm, {Steven W.} and Denney, {Maddie K.} and Krausfeldt, {Lauren E.} and Stough, {Joshua M.A.} and Meyer, {Kevin A.} and Dick, {Gregory J.} and Johengen, {Thomas H.} and Erika Lindquist and Tringe, {Susannah G.} and McKay, {Robert Michael L.}",

note = "Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2019 Davenport, Neudeck, Matson, Bullerjahn, Davis, Wilhelm, Denney, Krausfeldt, Stough, Meyer, Dick, Johengen, Lindquist, Tringe and McKay.",

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Davenport, EJ, Neudeck, MJ, Matson, PG, Bullerjahn, GS, Davis, TW, Wilhelm, SW, Denney, MK, Krausfeldt, LE, Stough, JMA, Meyer, KA, Dick, GJ, Johengen, TH, Lindquist, E, Tringe, SG & McKay, RML 2019, 'Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)', Frontiers in Microbiology, vol. 10, 2081. https://doi.org/10.3389/fmicb.2019.02081

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T1 - Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)

AU - Davenport, Emily J.

AU - Neudeck, Michelle J.

AU - Matson, Paul G.

AU - Bullerjahn, George S.

AU - Davis, Timothy W.

AU - Wilhelm, Steven W.

AU - Denney, Maddie K.

AU - Krausfeldt, Lauren E.

AU - Stough, Joshua M.A.

AU - Meyer, Kevin A.

AU - Dick, Gregory J.

AU - Johengen, Thomas H.

AU - Lindquist, Erika

AU - Tringe, Susannah G.

AU - McKay, Robert Michael L.

PY - 2019/9/10

Y1 - 2019/9/10

N2 - This study examined diel shifts in metabolic functions of Microcystis spp. during a 48-h Lagrangian survey of a toxin-producing cyanobacterial bloom in western Lake Erie in the aftermath of the 2014 Toledo Water Crisis. Transcripts mapped to the genomes of recently sequenced lower Great Lakes Microcystis isolates showed distinct patterns of gene expression between samples collected across day (10:00 h, 16:00 h) and night (22:00 h, 04:00 h). Daytime transcripts were enriched in functions related to Photosystem II (e.g., psbA), nitrogen and phosphate acquisition, cell division (ftsHZ), heat shock response (dnaK, groEL), and uptake of inorganic carbon (rbc, bicA). Genes transcribed during nighttime included those involved in phycobilisome protein synthesis and Photosystem I core subunits. Hierarchical clustering and principal component analysis (PCA) showed a tightly clustered group of nighttime expressed genes, whereas daytime transcripts were separated from each other over the 48-h duration. Lack of uniform clustering within the daytime transcripts suggested that the partitioning of gene expression in Microcystis is dependent on both circadian regulation and physicochemical changes within the environment.

AB - This study examined diel shifts in metabolic functions of Microcystis spp. during a 48-h Lagrangian survey of a toxin-producing cyanobacterial bloom in western Lake Erie in the aftermath of the 2014 Toledo Water Crisis. Transcripts mapped to the genomes of recently sequenced lower Great Lakes Microcystis isolates showed distinct patterns of gene expression between samples collected across day (10:00 h, 16:00 h) and night (22:00 h, 04:00 h). Daytime transcripts were enriched in functions related to Photosystem II (e.g., psbA), nitrogen and phosphate acquisition, cell division (ftsHZ), heat shock response (dnaK, groEL), and uptake of inorganic carbon (rbc, bicA). Genes transcribed during nighttime included those involved in phycobilisome protein synthesis and Photosystem I core subunits. Hierarchical clustering and principal component analysis (PCA) showed a tightly clustered group of nighttime expressed genes, whereas daytime transcripts were separated from each other over the 48-h duration. Lack of uniform clustering within the daytime transcripts suggested that the partitioning of gene expression in Microcystis is dependent on both circadian regulation and physicochemical changes within the environment.

KW - Lake Erie

KW - Microcystis

KW - cyanobacterial blooms

KW - metatranscriptomics

KW - microcystin

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U2 - 10.3389/fmicb.2019.02081

DO - 10.3389/fmicb.2019.02081

M3 - Article

AN - SCOPUS:85072838525

SN - 1664-302X

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

M1 - 2081

ER -

Metatranscriptomic Analyses of Diel Metabolic Functions During a Microcystis Bloom in Western Lake Erie (United States)

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Keywords

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