skip to main content


Title: Virus‐induced spore formation as a defense mechanism in marine diatoms
Summary

Algal viruses are important contributors to carbon cycling, recycling nutrients and organic material through host lysis. Although viral infection has been described as a primary mechanism of phytoplankton mortality, little is known about host defense responses.

We show that viral infection of the bloom‐forming, planktonic diatomChaetoceros socialisinduces the mass formation of resting spores, a heavily silicified life cycle stage associated with carbon export due to rapid sinking.

Although viral RNA was detected within spores, mature virions were not observed. ‘Infected’ spores were capable of germinating, but did not propagate or transmit infectious viruses.

These results demonstrate that diatom spore formation is an effective defense strategy against viral‐mediated mortality. They provide a possible mechanistic link between viral infection, bloom termination, and mass carbon export events and highlight an unappreciated role of viruses in regulating diatom life cycle transitions and ecological success.

 
more » « less
Award ID(s):
2021032
PAR ID:
10452391
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
New Phytologist
Volume:
229
Issue:
4
ISSN:
0028-646X
Page Range / eLocation ID:
p. 2251-2259
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Transmission from one host to another is a crucial component of parasite fitness. For some aquatic parasites, transmission occurs via a free‐living stage that spends time in the water, awaiting an encounter with a new host. These parasite transmission stages can be impacted by biotic and abiotic factors that influence the parasite's ability to successfully infect or grow in a new host.

    Here we tested whether time spent in the water column and/or exposure to common cyanobacterial toxins impacted parasite transmission stages. More specifically, we tested whether the infectivity, within host growth, and virulence of the fungal parasiteMetschnikowia bicuspidatachanged as a result of time spent in the water or from exposure to cyanotoxins in the water column. We exposed parasite transmission spores to different levels of one of two ecologically important cyanotoxins, microcystin‐LR and anatoxin‐a, and factorially manipulated the amount of time spores were incubated in water. We removed the toxins and used those same spores to infect one genotype of the common lake zooplanktonDaphnia dentifera.

    We found that cyanotoxins did not impact parasite fitness (infection prevalence and spore yield per infected host) or virulence (host lifetime reproduction and survivorship) at the tested concentrations (10 and 30 μg/L). However, we found that spending longer as a transmission spore decreased a spore's chances for successful infection: spores that were only incubated for 24 hr infected approximately 75% of exposed hosts, whereas spores incubated for 10 days infected less than 50% of exposed hosts.

    We also found a negative relationship between the final spore yield from infected hosts and the proportion of hosts that became infected. In treatments where spores spent longer in the water column prior to encountering a host, infection prevalence was lower (indicating lower per spore infectivity), but each infected host yielded more spores at the end of infection. We hypothesise that this pattern may result from intraspecific parasite competition within the host.

    Overall, these results suggest that transmission spores of this parasite are not strongly influenced by cyanotoxins in the water column, but that other aspects of spending time in the water strongly influence parasite fitness.

     
    more » « less
  2. Abstract

    Identifying patterns of pathogen infection in natural systems is crucial to understanding mechanisms of host–pathogen interactions. In this study, we explored how Junonia coenia densovirus (JcDV) infection varies over space and time in populations of the Melissa blue butterfly (Lycaeides melissa: Lycaenidae) using two different host plants. Collections ofL. melissaadults from multiple populations and years, along with host plant tissue and community samples of arthropods found on host plants, were screened to determine JcDV prevalence and load. Additionally, we sampled at multiple time points within a singleL. melissaflight season to investigate intra‐annual variation in infection patterns.

    We found population‐specific variation in viral prevalence ofL. melissaacross collection years, with historical samples potentially having higher viral prevalence than contemporary samples, although host plant diet was not informative for these patterns. Patterns of infection across multiple generations within a flight season showed that late‐season samples had a higher proportion of JcDV‐positive individuals, suggesting an accumulation of virus over the season. Sequence data from a segment of the JcDV capsid gene showed a lack of viral genetic diversity betweenL. melissacollected from different localities, and little to no viral particles were found in the surrounding environment.

    Our discovery of temporal variation in infection suggests that multiple sampling efforts must be made when describing pathogen prevalence in multivoltine hosts. Our findings represent an important first step towards further exploration of the ecological factors mediating disease prevalence and host‐specific variability of infection in wild insect populations.

     
    more » « less
  3. Abstract

    Determining parameters that govern pathogen transmission (such as the force of infection, FOI), and pathogen impacts on morbidity and mortality, is exceptionally challenging for wildlife. Vital parameters can vary, for example across host populations, between sexes and within an individual's lifetime.

    Feline immunodeficiency virus (FIV) is a lentivirus affecting domestic and wild cat species, forming species‐specific viral–host associations. FIV infection is common in populations of puma (Puma concolor), yet uncertainty remains over transmission parameters and the significance of FIV infection for puma mortality. In this study, the age‐specific FOI of FIV in pumas was estimated from prevalence data, and the evidence for disease‐associated mortality was assessed.

    We fitted candidate models to FIV prevalence data and adopted a maximum likelihood method to estimate parameter values in each model. The models with the best fit were determined to infer the most likely FOI curves. We applied this strategy for female and male pumas from California, Colorado, and Florida.

    When splitting the data by sex and area, our FOI modeling revealed no evidence of disease‐associated mortality in any population. Both sex and location were found to influence the FOI, which was generally higher for male pumas than for females. For female pumas at all sites, and male pumas from California and Colorado, the FOI did not vary with puma age, implying FIV transmission can happen throughout life; this result supports the idea that transmission can occur from mothers to cubs and also throughout adult life. For Florida males, the FOI was a decreasing function of puma age, indicating an increased risk of infection in the early years, and a decreased risk at older ages.

    This research provides critical insight into pathogen transmission and impact in a secretive and solitary carnivore. Our findings shed light on the debate on whether FIV causes mortality in wild felids like puma, and our approach may be adopted for other diseases and species. The methodology we present can be used for identifying likely transmission routes of a pathogen and also estimating any disease‐associated mortality, both of which can be difficult to establish for wildlife diseases in particular.

     
    more » « less
  4. Abstract

    For energetically limited organisms, life‐history theory predicts trade‐offs between reproductive effort and somatic maintenance. This is especially true of female mammals, for whom reproduction presents multifarious energetic and physiological demands.

    Here, we examine longitudinal changes in the gut virome (viral community) with respect to reproductive status in wild mature female chimpanzeesPan troglodytes schweinfurthiifrom two communities, Kanyawara and Ngogo, in Kibale National Park, Uganda.

    We used metagenomic methods to characterize viromes of individual chimpanzees while they were cycling, pregnant and lactating.

    Females from Kanyawara, whose territory abuts the park's boundary, had higher viral richness and loads (relative quantity of viral sequences) than females from Ngogo, whose territory is more energetically rich and located farther from large human settlements. Viral richness (total number of distinct viruses per sample) was higher when females were lactating than when cycling or pregnant. In pregnant females, viral richness increased with estimated day of gestation. Richness did not vary with age, in contrast to prior research showing increased viral abundance in older males from these same communities.

    Our results provide evidence of short‐term physiological trade‐offs between reproduction and infection, which are often hypothesized to constrain health in long‐lived species.

     
    more » « less
  5. Lauritano, Chiara ; Ianora, Adrianna (Ed.)

    Ecophysiological stress and the grazing of diatoms are known to elicit the production of chemical defense compounds called oxylipins, which are toxic to a wide range of marine organisms. Here we show that (1) the viral infection and lysis of diatoms resulted in oxylipin production; (2) the suite of compounds produced depended on the diatom host and the infecting virus; and (3) the virus-mediated oxylipidome was distinct, in both magnitude and diversity, from oxylipins produced due to stress associated with the growth phase. We used high-resolution accurate-mass mass spectrometry to observe changes in the dissolved lipidome of diatom cells infected with viruses over 3 to 4 days, compared to diatom cells in exponential, stationary, and decline phases of growth. Three host virus pairs were used as model systems: Chaetoceros tenuissimus infected with CtenDNAV; C. tenuissimus infected with CtenRNAV; and Chaetoceros socialis infected with CsfrRNAV. Several of the compounds that were significantly overproduced during viral infection are known to decrease the reproductive success of copepods and interfere with microzooplankton grazing. Specifically, oxylipins associated with allelopathy towards zooplankton from the 6-, 9-, 11-, and 15-lipogenase (LOX) pathways were significantly more abundant during viral lysis. 9-hydroperoxy hexadecatetraenoic acid was identified as the strongest biomarker for the infection of Chaetoceros diatoms. C. tenuissimus produced longer, more oxidized oxylipins when lysed by CtenRNAV compared to CtenDNAV. However, CtenDNAV caused a more statistically significant response in the lipidome, producing more oxylipins from known diatom LOX pathways than CtenRNAV. A smaller set of compounds was significantly more abundant in stationary and declining C. tenuissimus and C. socialis controls. Two allelopathic oxylipins in the 15-LOX pathway and essential fatty acids, arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) were more abundant in the stationary phase than during the lysis of C. socialis. The host–virus pair comparisons underscore the species-level differences in oxylipin production and the value of screening more host–virus systems. We propose that the viral infection of diatoms elicits chemical defense via oxylipins which deters grazing with downstream trophic and biogeochemical effects.

     
    more » « less