Cyanophage Propagation in the Freshwater Cyanobacterium Phormidium Is Constrained by Phosphorus Limitation and Enhanced by Elevated pCO2

Abstract

Intensification of human activities has led to changes in the availabilities of CO 2 and nutrients in freshwater ecosystems, which may greatly alter the physiological status of phytoplankton. Viruses require hosts for their reproduction and shifts in phytoplankton host physiology through global environmental change may thus affect viral infections as well. Various studies have investigated the impacts of single environmental factors on phytoplankton virus propagation, yet little is known about the impacts of multiple factors, particularly in freshwater systems. We therefore tested the combined effects of phosphorus limitation and elevated p CO 2 on the propagation of a cyanophage infecting a freshwater cyanobacterium. To this end, we cultured Phormidium in P-limited chemostats under ambient (400 μatm) and elevated (800 μatm) p CO 2 at growth rates of 0.6, 0.3, and 0.05 d -1 . Host C:P ratios generally increased with strengthened P-limitation and with elevated p CO 2 . Upon host steady state conditions, virus growth characteristics were obtained in separate infection assays where hosts were infected by the double-stranded DNA cyanophage PP. Severe P-limitation (host growth 0.05 d -1 ) led to a 85% decrease in cyanophage production rate and a 73% decrease in burst size compared to the 0.6 d -1 grown P-limited cultures. Elevated p CO 2 induced a 96% increase in cyanophage production rate and a 57% increase in burst size, as well as an 85% shorter latent period as compared to ambient p CO 2 at the different host growth rates. In addition, elevated p CO 2 caused a decrease in the plaquing efficiency and an increase in the abortion percentage for the 0.05 d -1 P-limited treatment, while the plaquing efficiency increased for the 0.6 d -1 P-limited cultures. Together, our results demonstrate interactive effects of elevated p CO 2 and P-limitation on cyanophage propagation, and show that viral propagation is generally constrained by P-limitation but enhanced with elevated p CO 2 . Our findings indicate that global change will likely have a severe impact on virus growth characteristics and thereby on the control of cyanobacterial hosts in freshwater ecosystems.

Warming advances virus population dynamics in a temperate freshwater plankton community

“…These conditions primarily affect host physiology, and thereby may influence virus replication or infection success. For example, earlier work has shown that under resource limitation host growth can be constrained, thereby prolonging virus latent period and/or resulting in a reduced burst size Cheng et al 2019). Warming has been reported to stimulate host growth rates and, as such, virus production (Steenhauer et al 2016;Demory et al 2017;Maat et al 2017).…”

Detection of bacteriophages and cyanophages for water quality control of a water supply system in Amazônia

“…This founding contributes as an important indicator of the interference of these phages in the environment, known for their ability to perform photosynthesis by consuming oxygen and their potential for binding to nitrogen or production of toxins [31]. Nitrogen or phosphorus supplies, in addition to reduced growth rate and biomass, may naturally limit freshwater ecosystems, including those involving cyanobacteria accumulation [35].…”

Toxic benthic freshwater cyanobacterial proliferations: Challenges and solutions for enhancing knowledge and improving monitoring and mitigation

“…Approximately 25% of all virus‐like particles (viruses that have not been cultured to determine host specificity) in the Gulf of Mexico are specific to the planktonic cyanobacterium Synechococcus (discussed in Hewson, O'Neil, & Dennison, 2001). There is limited information on viruses targeting benthic proliferations (Cheng, Frenken, Brussaard, & Van de Waal, 2019; Hewson et al, 2001; Voorhies et al., 2016). Of the few studies on benthic proliferations, Hewson et al.…”

“…(2001) identified virus‐like particles that were associated with a decline in Lyngbya majuscula Harvey ex Gomont in Moreton Bay, Australia, noting that further research was needed to understand the consequences of cyanophage‐mediated collapse within these communities. Additionally, Cheng et al (2019) assessed cyanophage infection through alterations in environmental stressors (phosphorus limitation and elevated pCO 2 ) in Phormidium . They also found that cyanophage adsorption and production rate was greater under moderate phosphorus limitation in combination with elevated pCO 2 levels, these results suggest that viral propagation and activation could increase as CO 2 levels rise.…”