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Title: Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network

Abstract

Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found inmore » sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [3];  [1]; ORCiD logo [4]
  1. Univ. of California, Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States); Univ. of Duisburg-Essen, Essen (Germany)
  3. Univ. of California, Berkeley, CA (United States); Univ. of Wisconsin, Madison, WI (United States)
  4. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Chan Zuckerberg Biohub, San Francisco, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE
OSTI Identifier:
1564043
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 13; Journal Issue: 6; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Bouma-Gregson, Keith, Olm, Matthew R., Probst, Alexander J., Anantharaman, Karthik, Power, Mary E., and Banfield, Jillian F. Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network. United States: N. p., 2019. Web. doi:10.1038/s41396-019-0374-3.
Bouma-Gregson, Keith, Olm, Matthew R., Probst, Alexander J., Anantharaman, Karthik, Power, Mary E., & Banfield, Jillian F. Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network. United States. https://doi.org/10.1038/s41396-019-0374-3
Bouma-Gregson, Keith, Olm, Matthew R., Probst, Alexander J., Anantharaman, Karthik, Power, Mary E., and Banfield, Jillian F. Tue . "Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network". United States. https://doi.org/10.1038/s41396-019-0374-3. https://www.osti.gov/servlets/purl/1564043.
@article{osti_1564043,
title = {Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network},
author = {Bouma-Gregson, Keith and Olm, Matthew R. and Probst, Alexander J. and Anantharaman, Karthik and Power, Mary E. and Banfield, Jillian F.},
abstractNote = {Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found in sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks.},
doi = {10.1038/s41396-019-0374-3},
journal = {The ISME Journal},
number = 6,
volume = 13,
place = {United States},
year = {Tue Feb 26 00:00:00 EST 2019},
month = {Tue Feb 26 00:00:00 EST 2019}
}

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Works referenced in this record:

Host-Specificity and Dynamics in Bacterial Communities Associated with Bloom-Forming Freshwater Phytoplankton
journal, January 2014


Attached Algae: The Cryptic Base of Inverted Trophic Pyramids in Freshwaters
journal, November 2017


Widespread anatoxin-a detection in benthic cyanobacterial mats throughout a river network
journal, May 2018


Chemical composition and production of exopolysaccharides from representative members of heterocystous and non-heterocystous cyanobacteria
journal, October 1999


The role of nitrogen and phosphorus in regulating Phormidium sp. (cyanobacteria) growth and anatoxin production
journal, February 2016

  • Heath, Mark; Wood, Susie A.; Young, Roger G.
  • FEMS Microbiology Ecology, Vol. 92, Issue 3
  • DOI: 10.1093/femsec/fiw021

Entrapped Sediments as a Source of Phosphorus in Epilithic Cyanobacterial Proliferations in Low Nutrient Rivers
journal, October 2015


Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria
text, January 2014


Successional Change in Microbial Communities of Benthic Phormidium-Dominated Biofilms
journal, December 2014


UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007


Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions
journal, June 2017


Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change
journal, April 2011


Data, information, knowledge and principle: back to metabolism in KEGG
journal, November 2013

  • Kanehisa, Minoru; Goto, Susumu; Sato, Yoko
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1076

Comparative Metagenomics of Toxic Freshwater Cyanobacteria Bloom Communities on Two Continents
journal, August 2012


Anatoxin-a Synthetase Gene Cluster of the Cyanobacterium Anabaena sp. Strain 37 and Molecular Methods To Detect Potential Producers
journal, August 2011

  • Rantala-Ylinen, Anne; Känä, Suvi; Wang, Hao
  • Applied and Environmental Microbiology, Vol. 77, Issue 20
  • DOI: 10.1128/aem.06022-11

A review of current knowledge on toxic benthic freshwater cyanobacteria – Ecology, toxin production and risk management
journal, October 2013


Microbial communities reflect temporal changes in cyanobacterial composition in a shallow ephemeral freshwater lake
journal, December 2015

  • Woodhouse, Jason Nicholas; Kinsela, Andrew Stephen; Collins, Richard Nicholas
  • The ISME Journal, Vol. 10, Issue 6
  • DOI: 10.1038/ismej.2015.218

Planktic Tychonema (Cyanobacteria) in the large lakes south of the Alps: phylogenetic assessment and toxigenic potential
journal, July 2016

  • Salmaso, Nico; Cerasino, Leonardo; Boscaini, Adriano
  • FEMS Microbiology Ecology, Vol. 92, Issue 10
  • DOI: 10.1093/femsec/fiw155

Metagenomic Identification of Bacterioplankton Taxa and Pathways Involved in Microcystin Degradation in Lake Erie
journal, April 2013


Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria
journal, January 2014


First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand
journal, August 2007


Microbial species delineation using whole genome sequences
journal, July 2015

  • Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
  • Nucleic Acids Research, Vol. 43, Issue 14
  • DOI: 10.1093/nar/gkv657

The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa
journal, January 2014

  • Rigosi, Anna; Carey, Cayelan C.; Ibelings, Bas W.
  • Limnology and Oceanography, Vol. 59, Issue 1
  • DOI: 10.4319/lo.2014.59.1.0099

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Nutrient and Light Limitation of Algae in two Northern California Streams
journal, June 1988


Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls
journal, January 2013


Identification of a Polyketide Synthase Coding Sequence Specific for Anatoxin-a-Producing Oscillatoria Cyanobacteria
journal, May 2009

  • Cadel-Six, S.; Iteman, I.; Peyraud-Thomas, C.
  • Applied and Environmental Microbiology, Vol. 75, Issue 14
  • DOI: 10.1128/AEM.02478-08

Seasonal Reassembly of a River food web: Floods, Droughts, and Impacts of fish
journal, May 2008

  • Power, Mary E.; Parker, Michael S.; Dietrich, William E.
  • Ecological Monographs, Vol. 78, Issue 2
  • DOI: 10.1890/06-0902.1

Dihydroanatoxin-a Is Biosynthesized from Proline in Cylindrospermum stagnale PCC 7417: Isotopic Incorporation Experiments and Mass Spectrometry Analysis
journal, June 2016


Sensitivity of Two Disjunct Bacterioplankton Communities to Exudates from the Cyanobacterium Microcystis aeruginosa Kützing
journal, July 2000


A genome-wide association study of seed protein and oil content in soybean
journal, January 2014


Ecological genomics meets community-level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation
journal, September 2014

  • Fitzpatrick, Matthew C.; Keller, Stephen R.
  • Ecology Letters, Vol. 18, Issue 1
  • DOI: 10.1111/ele.12376

Drainage from the Critical Zone: Lithologic Controls on the Persistence and Spatial Extent of Wetted Channels during the Summer Dry Season
journal, August 2018

  • Lovill, S. M.; Hahm, W. J.; Dietrich, W. E.
  • Water Resources Research, Vol. 54, Issue 8
  • DOI: 10.1029/2017WR021903

The ecology and biogeochemistry of stream biofilms
journal, March 2016

  • Battin, Tom J.; Besemer, Katharina; Bengtsson, Mia M.
  • Nature Reviews Microbiology, Vol. 14, Issue 4
  • DOI: 10.1038/nrmicro.2016.15

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Benthic bacterial diversity from freshwater tufas of the Iberian Range (Spain)
journal, February 2012


Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment
journal, May 2007


Flat laminated microbial mat communities
journal, October 2009


Mating pair stabilization mediates bacterial conjugation species specificity
journal, June 2022


The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists
journal, May 2016


Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene
journal, February 2015

  • Taranu, Zofia E.; Gregory-Eaves, Irene; Leavitt, Peter R.
  • Ecology Letters, Vol. 18, Issue 4
  • DOI: 10.1111/ele.12420

Revisiting the STEC Testing Approach: Using espK and espV to Make Enterohemorrhagic Escherichia coli (EHEC) Detection More Reliable in Beef
journal, January 2016


Genotypic and phenotypic analysis of strains assigned to the widespread cyanobacterial morphospecies Phormidium autumnale (Oscillatoriales)
journal, November 2007


Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development
journal, March 2015


Climate change: a catalyst for global expansion of harmful cyanobacterial blooms
journal, February 2009


The geographical structure of British bird distributions: diversity, spatial turnover and scale
journal, November 2001


Dihydroanatoxin-a Is Biosynthesized from Proline in Cylindrospermum stagnale PCC 7417: Isotopic Incorporation Experiments and Mass Spectrometry Analysis
journal, June 2016


The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms
journal, April 2016


Characterising and predicting cyanobacterial blooms in an 8-year amplicon sequencing time course
journal, May 2017

  • Tromas, Nicolas; Fortin, Nathalie; Bedrani, Larbi
  • The ISME Journal, Vol. 11, Issue 8
  • DOI: 10.1038/ismej.2017.58

Metagenomic Identification of Bacterioplankton Taxa and Pathways Involved in Microcystin Degradation in Lake Erie
journal, April 2013


Pharmacology of Anatoxin-a, produced by the freshwater cyanophyte Anabaena flos-aquae NRC-44-1
journal, January 1979


Benthic freshwater cyanobacteria as indicators of anthropogenic pressures
journal, August 2016


Are We Underestimating Benthic Cyanotoxins? Extensive Sampling Results from Spain
journal, November 2017

  • Cantoral Uriza, Enrique; Asencio, Antonia; Aboal, Marina
  • Toxins, Vol. 9, Issue 12
  • DOI: 10.3390/toxins9120385

Several problems of the polyphasic approach in the modern cyanobacterial system
journal, October 2017


Ecological genomics meets community-level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation
journal, September 2014

  • Fitzpatrick, Matthew C.; Keller, Stephen R.
  • Ecology Letters, Vol. 18, Issue 1
  • DOI: 10.1111/ele.12376

Wadeable streams as widespread sources of benthic cyanotoxins in California, USA
journal, November 2015


The high resilience of the bacterioplankton community in the face of a catastrophic disturbance by a heavy Microcystis bloom
journal, June 2012


SIGNIFICANCE OF BACTERIAL-ANABAENA (CYANOPHYCEAE) ASSOCIATIONS WITH RESPECT TO N 2 FIXATION IN FRESHWATER 2
journal, September 1978


Polyphasic approach and typification of selected Phormidium strains (Cyanobacteria)
journal, December 2011


Food webs in Mediterranean rivers
journal, May 2013


Host-Specificity and Dynamics in Bacterial Communities Associated with Bloom-Forming Freshwater Phytoplankton
journal, January 2014


Widespread anatoxin-a detection in benthic cyanobacterial mats throughout a river network
journal, May 2018


Attached Algae: The Cryptic Base of Inverted Trophic Pyramids in Freshwaters
journal, November 2017


Entrapped Sediments as a Source of Phosphorus in Epilithic Cyanobacterial Proliferations in Low Nutrient Rivers
journal, October 2015


Stoichiometric regulation of phytoplankton toxins
journal, April 2014

  • Van de Waal, Dedmer B.; Smith, Val H.; Declerck, Steven A. J.
  • Ecology Letters, Vol. 17, Issue 6
  • DOI: 10.1111/ele.12280

Bacteria and diatom co-occurrence patterns in microbial mats from polar desert streams: Diatom : bacteria co-occurrence in Dry Valley streams
journal, September 2012


Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions
journal, June 2017


A review of current knowledge on toxic benthic freshwater cyanobacteria – Ecology, toxin production and risk management
journal, October 2013


Algal mats and insect emergence in rivers under Mediterranean climates: towards photogrammetric surveillance
journal, October 2009


High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms
journal, November 2008

  • Berg, Katri A.; Lyra, Christina; Sivonen, Kaarina
  • The ISME Journal, Vol. 3, Issue 3
  • DOI: 10.1038/ismej.2008.110

Assessment of potential reference sites for evaluating the ecological status of subtropical and temperate Brazilian lotic systems using the epilithic diatom community
journal, October 2020

  • Freitas, Núbia Cristina Weber; Heinrich, Carla Giselda; Etges, Tanise
  • Environmental Science and Pollution Research, Vol. 28, Issue 7
  • DOI: 10.1007/s11356-020-11136-w

The role of nitrogen and phosphorus in regulating Phormidium sp. (cyanobacteria) growth and anatoxin production
journal, February 2016

  • Heath, Mark; Wood, Susie A.; Young, Roger G.
  • FEMS Microbiology Ecology, Vol. 92, Issue 3
  • DOI: 10.1093/femsec/fiw021

Bacterial phosphate metabolism and its application to phosphorus recovery and industrial bioprocesses
journal, May 2010

  • Hirota, Ryuichi; Kuroda, Akio; Kato, Junichi
  • Journal of Bioscience and Bioengineering, Vol. 109, Issue 5
  • DOI: 10.1016/j.jbiosc.2009.10.018

The cultivation of myxophyceae
journal, January 1952


Microbial species delineation using whole genome sequences
journal, July 2015

  • Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
  • Nucleic Acids Research, Vol. 43, Issue 14
  • DOI: 10.1093/nar/gkv657

The Abundance of Toxic Genotypes Is a Key Contributor to Anatoxin Variability in Phormidium-Dominated Benthic Mats
journal, October 2017

  • Wood, Susanna; Puddick, Jonathan
  • Marine Drugs, Vol. 15, Issue 10
  • DOI: 10.3390/md15100307

Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls
journal, January 2013


UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007


Successional Change in Microbial Communities of Benthic Phormidium-Dominated Biofilms
journal, December 2014


Light-mediated thresholds in stream-water nutrient composition in a river network
journal, January 2011

  • Finlay, Jacques C.; Hood, James M.; Limm, Michael P.
  • Ecology, Vol. 92, Issue 1
  • DOI: 10.1890/09-2243.1

Microbial communities reflect temporal changes in cyanobacterial composition in a shallow ephemeral freshwater lake
journal, December 2015

  • Woodhouse, Jason Nicholas; Kinsela, Andrew Stephen; Collins, Richard Nicholas
  • The ISME Journal, Vol. 10, Issue 6
  • DOI: 10.1038/ismej.2015.218

Anatoxin- a , a toxic alkaloid from Anabaena flos-aquae NRC-44h
journal, April 1977

  • Devlin, J. P.; Edwards, O. E.; Gorham, P. R.
  • Canadian Journal of Chemistry, Vol. 55, Issue 8
  • DOI: 10.1139/v77-189

Biosynthesis of anatoxin-a and analogues (anatoxins) in cyanobacteria
journal, December 2014


The high resilience of the bacterioplankton community in the face of a catastrophic disturbance by a heavy Microcystis bloom
journal, June 2012


Diagnosis of Anatoxin-a Poisoning in Dogs from North America
journal, January 2008

  • Puschner, Birgit; Hoff, Brent; Tor, Elizabeth R.
  • Journal of Veterinary Diagnostic Investigation, Vol. 20, Issue 1
  • DOI: 10.1177/104063870802000119

Hierarchical Grouping to Optimize an Objective Function
journal, March 1963


Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, Cyanobacteria)
journal, November 2013

  • Strunecký, Otakar; Komárek, Jiří; Johansen, Jeffrey
  • Journal of Phycology, Vol. 49, Issue 6
  • DOI: 10.1111/jpy.12128

Poisonous Australian Lake
journal, May 1878


IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012


Molecular and morphological criteria for revision of the genus Microcoleus (Oscillatoriales, Cyanobacteria)
journal, November 2013

  • Strunecký, Otakar; Komárek, Jiří; Johansen, Jeffrey
  • Journal of Phycology, Vol. 49, Issue 6
  • DOI: 10.1111/jpy.12128

Within-Mat Variability in Anatoxin-a and Homoanatoxin-a Production among Benthic Phormidium (Cyanobacteria) Strains
journal, October 2012

  • Wood, Susanna A.; Smith, Francine M. J.; Heath, Mark W.
  • Toxins, Vol. 4, Issue 10
  • DOI: 10.3390/toxins4100900

Food webs in Mediterranean rivers
journal, May 2013


Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment
journal, May 2007


Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils
journal, October 2013

  • Sharma, Seema B.; Sayyed, Riyaz Z.; Trivedi, Mrugesh H.
  • SpringerPlus, Vol. 2, Issue 1
  • DOI: 10.1186/2193-1801-2-587

The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists
journal, May 2016


Measuring beta diversity for presence-absence data
journal, May 2003


First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand
journal, August 2007


Sensitivity of Two Disjunct Bacterioplankton Communities to Exudates from the Cyanobacterium Microcystis aeruginosa Kützing
journal, July 2000


Within-Mat Variability in Anatoxin-a and Homoanatoxin-a Production among Benthic Phormidium (Cyanobacteria) Strains
journal, October 2012

  • Wood, Susanna A.; Smith, Francine M. J.; Heath, Mark W.
  • Toxins, Vol. 4, Issue 10
  • DOI: 10.3390/toxins4100900

Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene
journal, February 2015

  • Taranu, Zofia E.; Gregory-Eaves, Irene; Leavitt, Peter R.
  • Ecology Letters, Vol. 18, Issue 4
  • DOI: 10.1111/ele.12420

Pharmacology of Anatoxin-a, produced by the freshwater cyanophyte Anabaena flos-aquae NRC-44-1
journal, January 1979


The ecology and biogeochemistry of stream biofilms
journal, March 2016

  • Battin, Tom J.; Besemer, Katharina; Bengtsson, Mia M.
  • Nature Reviews Microbiology, Vol. 14, Issue 4
  • DOI: 10.1038/nrmicro.2016.15

Effect of river flow, temperature, and water chemistry on proliferations of the benthic anatoxin-producing cyanobacterium Phormidium
journal, March 2017

  • Wood, Susanna A.; Atalah, Javier; Wagenhoff, Annika
  • Freshwater Science, Vol. 36, Issue 1
  • DOI: 10.1086/690114

The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms
journal, April 2016


Characterising and predicting cyanobacterial blooms in an 8-year amplicon sequencing time course
journal, May 2017

  • Tromas, Nicolas; Fortin, Nathalie; Bedrani, Larbi
  • The ISME Journal, Vol. 11, Issue 8
  • DOI: 10.1038/ismej.2017.58

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa
journal, January 2014

  • Rigosi, Anna; Carey, Cayelan C.; Ibelings, Bas W.
  • Limnology and Oceanography, Vol. 59, Issue 1
  • DOI: 10.4319/lo.2014.59.1.0099

Genotypic and phenotypic analysis of strains assigned to the widespread cyanobacterial morphospecies Phormidium autumnale (Oscillatoriales)
journal, November 2007


Biosynthesis of anatoxin-a and analogues (anatoxins) in cyanobacteria
journal, December 2014


Light-mediated thresholds in stream-water nutrient composition in a river network
journal, January 2011

  • Finlay, Jacques C.; Hood, James M.; Limm, Michael P.
  • Ecology, Vol. 92, Issue 1
  • DOI: 10.1890/09-2243.1

Hierarchical Grouping to Optimize an Objective Function
journal, March 1963

  • Ward, Joe H.
  • Journal of the American Statistical Association, Vol. 58, Issue 301
  • DOI: 10.2307/2282967

Generalized Additive Models
book, May 2017


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journal, June 2020


The rise of diversity in metabolic platforms across the Candidate Phyla Radiation
journal, June 2020

  • Jaffe, Alexander L.; Castelle, Cindy J.; Matheus Carnevali, Paula B.
  • BMC Biology, Vol. 18, Issue 1
  • DOI: 10.1186/s12915-020-00804-5

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journal, December 2019


The rise of diversity in metabolic platforms across the Candidate Phyla Radiation
journal, June 2020

  • Jaffe, Alexander L.; Castelle, Cindy J.; Matheus Carnevali, Paula B.
  • BMC Biology, Vol. 18, Issue 1
  • DOI: 10.1186/s12915-020-00804-5