Ecology
Research Article
12 September 2024

Virulence and transmission biology of the widespread, ecologically important pathogen of zooplankton, Spirobacillus cienkowskii

ABSTRACT

Spirobacillus cienkowskii (Spirobacillus, hereafter) is a widely distributed bacterial pathogen that has significant impacts on the population dynamics of zooplankton (Daphnia spp.), particularly in months when Daphnia are asexually reproducing. However, little is known about Spirobacillus’ virulence, transmission mode, and dynamics. As a result, we cannot explain the dynamics of Spirobacillus epidemics in nature or use Spirobacillus as a model pathogen, despite Daphnia’s tractability as a model host. Here, we work to fill these knowledge gaps experimentally. We found that Spirobacillus is among the most virulent of Daphnia pathogens, killing its host within a week and reducing host fecundity. We further found that Spirobacillus did not transmit horizontally among hosts unless the host died or was destroyed (i.e., it is an “obligate killer”). In experiments aimed at quantifying the dynamics of horizontal transmission among asexually reproducing Daphnia, we demonstrated that Spirobacillus transmits poorly in the laboratory. In mesocosms, Spirobacillus failed to generate epidemics; in experiments wherein individual Daphnia were exposed, Spirobacillus’ transmission success was low. In the (limited) set of conditions we considered, Spirobacillus’ transmission success did not change with host density or pathogen dose and declined following environmental incubation. Finally, we conducted a field survey of Spirobacillus’ prevalence within egg cases (ephippia) made by sexually reproducing Daphnia. We found Spirobacillus DNA in ~40% of ephippia, suggesting that, in addition to transmitting horizontally among asexually reproducing Daphnia, Spirobacillus may transmit vertically from sexually reproducing Daphnia. Our work fills critical gaps in the biology of Spirobacillus and illuminates new hypotheses vis-à-vis its life history.

IMPORTANCE

Spirobacillus cienkowskii is a bacterial pathogen of zooplankton, first described in the 19th century and recently placed in a new family of bacteria, the Silvanigrellaceae. Spirobacillus causes large epidemics in lake zooplankton populations and increases the probability that zooplankton will be eaten by predators. However, little is known about how Spirobacillus transmits among hosts, to what extent it reduces host survival and reproduction (i.e., how virulent it is), and what role virulence plays in Spirobacillus’ life cycle. Here, we experimentally quantified Spirobacillus’ virulence and showed that Spirobacillus must kill its host to transmit horizontally. We also found evidence that Spirobacillus may transmit vertically via Daphnia’s seed-like egg sacks. Our work will help scientists to (i) understand Spirobacillus epidemics, (ii) use Spirobacillus as a model pathogen for the study of host-parasite interactions, and (iii) better understand the unusual group of bacteria to which Spirobacillus belongs.

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REFERENCES

1.
Duncan AB, Little TJ. 2007. Parasite-driven genetic change in a natural population of Daphnia. Evolution 61:796–803.
2.
Duffy MA, Ochs JH, Penczykowski RM, Civitello DJ, Klausmeier CA, Hall SR. 2012. Ecological context influences epidemic size and parasite-driven evolution. Science 335:1636–1638.
3.
Duffy MA, Brassil CE, Hall SR, Tessier AJ, Cáceres CE, Conner JK. 2008. Parasite-mediated disruptive selection in a natural Daphnia population. BMC Evol Biol 8:80.
4.
Duffy MA, Hall SR, Tessier AJ, Huebner M. 2005. Selective predators and their parasitized prey: are epidemics in zooplankton under top-down control? Limnol Oceanogr 50:412–420.
5.
Johnson PTJ, Stanton DE, Preu ER, Forshay KJ, Carpenter SR. 2006. Dining on disease: how interactions between infection and environment affect predation risk. Ecology 87:1973–1980.
6.
Wale N, Fuller RC, Johnsen S, Turrill ML, Duffy MA. 2021. The visual ecology of selective predation: are unhealthy hosts less stealthy hosts? Ecol Evol 11:18591–18603.
7.
Ebert D. 2008. Host–parasite coevolution: insights from the Daphnia–parasite model system. Curr Opin Microbiol 11:290–301.
8.
Ebert D. 2022. Daphnia as a versatile model system in ecology and evolution. Evodevo 13:16.
9.
Hahn MW, Pitt A. 2017. Silvanigrella, p 1–9. In Bergey’s manual of systematics of archaea and bacteria
10.
Hahn MW, Schmidt J, Koll U, Rohde M, Verbarg S, Pitt A, Nakai R, Naganuma T, Lang E. 2017. Silvanigrella aquatica gen. nov., sp. nov., isolated from a freshwater lake, description of Silvanigrellaceae fam. nov. and Silvanigrellales ord. nov., reclassification of the order Bdellovibrionales in the class Oligoflexia, reclassification of the families Bacteriovoracaceae and Halobacteriovoraceae in the new order Bacteriovoracales ord. nov., and reclassification of the family Pseudobacteriovoracaceae in the order Oligoflexales. Int J Syst Evol Microbiol 67:2555–2568.
11.
Metchnikoff E. 1889. Contributions a l’etude du pleomorphisme des bacteriens. Annales de l’Institut Pasteur 3:61–68.
12.
Rodrigues JLM, Duffy MA, Tessier AJ, Ebert D, Mouton L, Schmidt TM. 2008. Phylogenetic characterization and prevalence of Spirobacillus cienkowskii, a red-pigmented, spiral-shaped bacterial pathogen of freshwater Daphnia species. Appl Environ Microbiol 74:1575–1582.
13.
Green J. 1959. Carotenoid pigment in Spirobacillus cienkowskii Metchnikoff, a pathogen of cladocera. Nature 183:56–57.
14.
Mioduchowska M, Czyż MJ, Gołdyn B, Kilikowska A, Namiotko T, Pinceel T, Łaciak M, Sell J. 2018. Detection of bacterial endosymbionts in freshwater crustaceans: the applicability of non-degenerate primers to amplify the bacterial 16S rRNA gene. PeerJ 6:e6039.
15.
Duffy MA, Hall SR. 2008. Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations. Am Nat 171:499–510.
16.
Hall SR, Duffy MA, Cáceres CE. 2005. Selective predation and productivity jointly drive complex behavior in host-parasite systems. Am Nat 165:70–81.
17.
Wale N, Turrill ML, Duffy MA. 2019. A colorful killer: Daphnia infected with the bacterium Spirobacillus cienkowskii exhibit unexpected color variation. Ecology 100:e02562.
18.
Ebert D, Rainey P, Embley TM, Scholz D. 1996. Development, life cycle, ultrastructure and phylogenetic position of Pasteuria ramosa Metchnikoff 1888: rediscovery of an obligate endoparasite of Daphnia magna straus. Phil Trans R Soc Lond B 351:1689–1701.
19.
McCallum H, Fenton A, Hudson PJ, Lee B, Levick B, Norman R, Perkins SE, Viney M, Wilson AJ, Lello J. 2017. Breaking beta: deconstructing the parasite transmission function. Philos Trans R Soc Lond B Biol Sci 372:20160084.
20.
Bjørnstad ON. 2023. Epidemics: models and data using R
21.
Cortez MH, Weitz JS. 2013. Distinguishing between indirect and direct modes of transmission using epidemiological time series. Am Nat 181:E43–E54.
22.
Turner WC, Kamath PL, van Heerden H, Huang Y-H, Barandongo ZR, Bruce SA, Kausrud K. 2021. The roles of environmental variation and parasite survival in virulence–transmission relationships. R Soc Open Sci 8:210088.
23.
Gandon S. 1998. The curse of the pharoah hypothesis. Proc Biol Sci 265:1545–1552.
24.
Li S, Eisenberg JNS, Spicknall IH, Koopman JS. 2009. Dynamics and control of infections transmitted from person to person through the environment. Am J Epidemiol 170:257–265.
25.
Ogbunugafor CB, Miller-Dickson MD, Meszaros VA, Gomez LM, Murillo AL, Scarpino SV. 2020. Variation in microparasite free-living survival and indirect transmission can modulate the intensity of emerging outbreaks. Sci Rep 10:20786.
26.
Rumschlag SL, Roth SA, McMahon TA, Rohr JR, Civitello DJ. 2022. Variability in environmental persistence but not per capita transmission rates of the amphibian chytrid fungus leads to differences in host infection prevalence. J Anim Ecol 91:170–181.
27.
Ebert D. 2005. Ecology,epidemiology, and evolution of parasitism in Daphnia. National Center for Biotechnology Information, NIH, Bethesda, MD.
28.
Keeling MJ, Rohani P. 2011. Modeling infectious diseases in humans and animals. Princeton University Press.
29.
Begon M, Bennett M, Bowers RG, French NP, Hazel SM, Turner J. 2002. A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiol Infect 129:147–153.
30.
Davenport ES, Dziuba MK, Jacobson LE, Calhoun SK, Monell KJ, Duffy MA. 2024. How does parasite environmental transmission stage concentration change before, during, and after disease outbreaks? Ecology 105:e4235.
31.
Gowler CD, Rogalski MA, Shaw CL, Hunsberger KK, Duffy MA. 2021. Density, parasitism, and sexual reproduction are strongly correlated in lake Daphnia populations. Ecol Evol 11:10446–10456.
32.
Rogalski MA, Leavitt PR, Skelly DK. 2017. Daphniid zooplankton assemblage shifts in response to eutrophication and metal contamination during the Anthropocene. Proc Biol Sci 284:20170865.
33.
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. 2012. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134.
34.
Field A, Miles J, Field Z. 2012. Discovering statistics using R. SAGE Publications Ltd.
35.
Bailey DM, Collins MA, Gordon JDM, Zuur AF, Priede IG. 2009. Long-term changes in deep-water fish populations in the northeast Atlantic: a deeper reaching effect of fisheries? Proc Biol Sci 276:1965–1969.
36.
Therneau TM. 2023. A package for survival analysis in R. Available from: https://CRAN.R-project.org/package=survival
37.
Therneau T, Crowson C, Atkinson E. Multi-state models and competing risks. Available from: https://cran.r-project.org/web/packages/survival/vignettes/compete.pdf. Retrieved 2022.
38.
Clay PA, Dhir K, Rudolf VHW, Duffy MA. 2019. Within-host priority effects systematically alter pathogen coexistence. Am Nat 193:187–199.
39.
Duffy MA, Cáceres CE, Hall SR. 2019. Healthy herds or predator spreaders? Insights from the plankton into how predators suppress and spread disease, p 458–479. In Wilson K, Fenton A, Tompkins D (ed), Wildlife disease ecology: linking theory to data and application. Cambridge University Press.
40.
Cáceres CE, Knight CJ, Hall SR. 2009. Predator–spreaders: predation can enhance parasite success in a planktonic host–parasite system. Ecology 90:2850–2858.
41.
Bresciani L, Lemos LN, Wale N, Lin JY, Strauss AT, Duffy MA, Rodrigues JLM. 2018. Draft genome sequence of “Candidatus Spirobacillus cienkowskii,” a pathogen of freshwater Daphnia species, reconstructed from hemolymph metagenomic reads. Microbiol Resour Announc 7:e01175-18.
42.
Tate AT. 2016. The interaction of immune priming with different modes of disease transmission. Front Microbiol 7:1102.
43.
Ben-Ami F, Regoes RR, Ebert D. 2008. A quantitative test of the relationship between parasite dose and infection probability across different hostparasite combinations. Proc Biol Sci 275:853–859.
44.
Ben-Ami F, Ebert D, Regoes RR. 2010. Pathogen dose infectivity curves as a method to analyze the distribution of host susceptibility: a quantitative assessment of maternal effects after food stress and pathogen exposure. Am Nat 175:106–115.
45.
Regoes RR, Hottinger JW, Sygnarski L, Ebert D. 2003. The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiology Amp Infect 131:957–966.
46.
Lunn TJ, Restif O, Peel AJ, Munster VJ, de Wit E, Sokolow S, van Doremalen N, Hudson P, McCallum H. 2019. Dose–response and transmission: the nexus between reservoir hosts, environment and recipient hosts. Philos Trans R Soc Lond B Biol Sci 374:20190016.
47.
Clay PA, Cortez MH, Duffy MA. 2021. Dose relationships can exacerbate, mute, or reverse the impact of heterospecific host density on infection prevalence. Ecology 102:e03422.
48.
Thomas S, Bertram C, van Rensburg K, Cáceres C, Duffy M. 2011. Spatiotemporal dynamics of free-living stages of a bacterial parasite of zooplankton. Aquat Microb Ecol 63:265–272.
49.
Wetzel RG. 2001. Light in inland waters, p 49–69. In Third. Elsevier.
50.
Morris RL, Schmidt TM. 2013. Shallow breathing: bacterial life at low O2. Nat Rev Microbiol 11:205–212.
51.
Sockett RE. 2009. Predatory lifestyle of Bdellovibrio bacteriovorus. Annu Rev Microbiol 63:523–539.
52.
Lutz C, Erken M, Noorian P, Sun S, McDougald D. 2013. Environmental reservoirs and mechanisms of persistence of Vibrio cholerae. Front Microbiol 4:375.
53.
O’Hara MB, Hageman JH. 1990. Energy and calcium ion dependence of proteolysis during sporulation of Bacillus subtilis cells. J Bacteriol 172:4161–4170.
54.
Pandey A, Mideo N, Platt TG. 2022. Virulence evolution of pathogens that can grow in reservoir environments. Am Nat 199:141–158.

Information & Contributors

Information

Published In

cover image Applied and Environmental Microbiology
Applied and Environmental Microbiology
Online First
eLocator: e01529-23
Editor: Pablo Tortosa, UMR Processus Infectieux en Milieu Insulaire Tropical, Ste. Clotilde, France
PubMed: 39264204

History

Received: 11 September 2023
Accepted: 1 June 2024
Published online: 12 September 2024

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Keywords

  1. Silvanigrellaceae
  2. disease ecology
  3. virulence
  4. transmission
  5. Daphnia
  6. environmental transmission

Data Availability

The data for this paper are available on Dryad at https://doi.org/10.5061/dryad.d51c5b0c4.

Contributors

Authors

Department of Microbiology, Genetics & Immunology, Michigan State University, East Lansing, Michigan, USA
Department of Integrative Biology, Michigan State University, East Lansing, Michigan, USA
Program in Ecology, Evolution and Behavior, Michigan State University, East Lansing, Michigan, USA
Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
Author Contributions: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, and Writing – review and editing.
Claire B. Freimark
Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
Author Contributions: Investigation and Methodology.
Present address: Department of Ecology & Evolutionary Biology, University of California Irvine, Irvine, California, USA
Justin Ramirez
Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
Author Contribution: Investigation.
Marcin K. Dziuba
Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
Author Contributions: Investigation and Writing – review and editing.
Ahmad Y. Kafri
Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
Author Contribution: Investigation.
Rebecca Bilich
Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
Author Contribution: Investigation.
Present address: School of Medicine, Wayne State University, Detroit, Michigan, USA
Meghan A. Duffy
Department of Ecology & Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA

Editor

Pablo Tortosa
Editor
UMR Processus Infectieux en Milieu Insulaire Tropical, Ste. Clotilde, France

Notes

The authors declare no conflict of interest.

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