Cyanotoxin impact on microbial-mediated nitrogen transformations at
the interface of sediment-water column in surface water bodies
Hanyan Li
a
, Marielle Hollstein
a
, Aditi Podder
a
, Vedansh Gupta
b
, Michael Barber
a
,
Ramesh Goel
a, *
a
Department of Civil and Environmental Engineering, University of Utah, UT, USA
b
Microvi Biotech Inc, Hayward, CA, USA
article info
Article history:
Received 30 April 2020
Received in revised form
23 July 2020
Accepted 26 July 2020
Available online 6 August 2020
This paper has been recommended for
acceptance by Markus Hauck.
Keywords:
Sediment interface
Reversible kinetics
Microcystin-LR
Nitrifiers
Kinetics
amoA gene
abstract
Harmful cyanobacterial blooms produce lethal toxins in many aquatic ecosystems experiencing eutro-
phication. This manuscript presents results on the effects of cyanotoxins on the aerobic microbial
communities residing at the interface of sediments and water columns with the ammonia-oxidizing
bacteria (AOB) as the model microbial community. Microcystin-LR (MC-LR), a heavily researched cya-
notoxin variant, was used as the model cyanotoxin. To measure cyanotoxin influence on the activity of
nitrifying microbial communities, an enriched culture of AOBs collected from an ongoing partial
nitrification-nitritation reactor was examined for its exposure to 1, 5 and 10 mg/L of MC-LR. The nitri-
tation kinetics experiment demonstrated MC-LR’s ability at 1, 5, and 10 mg/L concentrations to prevent
ammonium oxidation with statistically significant differences in nitritation rates between the blanks and
spiked samples (One-way ANOVA, p < 0.05). Significantly decreased dissolved oxygen (DO) consumption
during oxygen update batch tests demonstrated toxin’s influence on AOB’s oxidizing capabilities when
exposed to even lower concentrations of 0.75, 0.5, and 0.25 mg/L of MC-LR in a separate set of experi-
ments. Based on competitive kinetics, the MC-LR inhibition coefficient-the concentration needed to
produce half-maximum inhibition of the mixed community AOBs was determined to be 0.083 mg/L. The
stress tests proved the recovery of nitritation to some extent at lower MC-LR concentrations (1 and 5 mg/
L), but significant irreversible inhibition was recorded when the AOB population was exposed to 10 mg/L
MC-LR. The comparisons of amoA gene expressions corresponded well with nitrifying kinetics. All
concentrations of MC-LR spiking were determined to produce a discernible impact on the AOB nitritation
rate by either destroying the bacterial cell or immediately inhibiting the amoA gene expression.
© 2020 Elsevier Ltd. All rights reserved.
1. Introduction
Over the last few decades, the growth of harmful algal blooms
(HABs) in many aquatic systems has become a prevalent problem
due to increased agricultural runoff, wastewater treatment plant
effluents and other nonpoint source discharges with high concen-
trations of nutrients getting into lakes (Heisler et al., 2008). While
algal and cyanobacterial biomass occur naturally in aquatic eco-
systems, cyanobacterial blooms are amplified by anthropogenic
activities, such as excess agricultural, point and nonpoint run offs
(Paerl et al., 2011; Paerl and Otten, 2013). Cyanotoxins, which are
cyanobacterial secondary metabolites, are one of the most potent
contaminants found in freshwater ecosystems (Stewart et al.,
2008). Human, ecological and microbial health is affected by the
toxins produced by cyanobacteria. Microcystin-LR (MC-LR) is
mainly a dangerous cyanotoxin, known for accumulating in the
liver of humans, livestock, and other animals (Lone et al., 2015).
As recent studies demonstrate how climate change correlates to
cyanobacterial blooms (Wells et al., 2015; Griffith and Gobler,
2020), cyanotoxin’s ecological impact has become a predominant
question in relation to lake water post-bloom conditions (Dalu and
Wasserman, 2018). While lake water conditions during algal
blooms are toxic to the surrounding plant, animal, and microbial
species, long term effects of cyanobacterial blooms are more in-
definite. Moreover, cyanotoxin strains have appeared throughout
the water column, sediment, marine life, and even tertiary plants in
* Corresponding author.
E-mail address: ram.goel@utah.edu (R. Goel).
Contents lists available at ScienceDirect
Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol
https://doi.org/10.1016/j.envpol.2020.115283
0269-7491/© 2020 Elsevier Ltd. All rights reserved.
Environmental Pollution 266 (2020) 115283