Viral Chemotaxis of Paramecium Bursaria Altered by Algal Endosymbionts.
Chemotaxis
Chlorovirus
Ecological catalyst
Food webs
Giant virus
Nutrition
Protist
Symbiosis
Virotaxy
Virovory
Journal
Microbial ecology
ISSN: 1432-184X
Titre abrégé: Microb Ecol
Pays: United States
ID NLM: 7500663
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
22
05
2023
accepted:
23
08
2023
medline:
13
11
2023
pubmed:
31
8
2023
entrez:
31
8
2023
Statut:
ppublish
Résumé
Chemotaxis is widespread across many taxa and often aids resource acquisition or predator avoidance. Species interactions can modify the degree of movement facilitated by chemotaxis. In this study, we investigated the influence of symbionts on Paramecium bursaria's chemotactic behavior toward chloroviruses. To achieve this, we performed choice experiments using chlorovirus and control candidate attractors (virus stabilization buffer and pond water). We quantified the movement of Paramecia grown with or without algal and viral symbionts toward each attractor. All Paramecia showed some chemotaxis toward viruses, but cells without algae and viruses showed the most movement toward viruses. Thus, the endosymbiotic algae (zoochlorellae) appeared to alter the movement of Paramecia toward chloroviruses, but it was not clear that ectosymbiotic viruses (chlorovirus) also had this effect. The change in behavior was consistent with a change in swimming speed, but a change in attraction remains possible. The potential costs and benefits of chemotactic movement toward chloroviruses for either the Paramecia hosts or its symbionts remain unclear.
Identifiants
pubmed: 37650927
doi: 10.1007/s00248-023-02292-w
pii: 10.1007/s00248-023-02292-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2904-2909Subventions
Organisme : Directorate for Biological Sciences
ID : 1736030
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Brown JA, Nielsen PJ (1974) Transfer of photosynthetically produced carbohydrate from endosymbiotic chlorellae to Paramecium bursaria. J Protozool 21(4):569–570. https://doi.org/10.1111/j.1550-7408.1974.tb03702.x
doi: 10.1111/j.1550-7408.1974.tb03702.x
Bulannga RB, Schmidt S (2023) Two predators, one prey—the interaction between bacteriophage, bacterivorous ciliates, and Escherichia coli. Microb Ecol. https://doi.org/10.1007/s00248-022-02163-w
doi: 10.1007/s00248-022-02163-w
pubmed: 36723682
DeLong JP, Al-Ameeli Z, Duncan G, Van Etten JL, Dunigan DD (2016) Predators catalyze an increase in chloroviruses by foraging on the symbiotic hosts of zoochlorellae. Proc Natl Acad Sci 113(48):13780–13784. https://doi.org/10.1073/pnas.1613843113
doi: 10.1073/pnas.1613843113
pubmed: 27821770
pmcid: 5137705
DeLong JP, Van Etten JL, Al-Ameeli Z, Agarkova IV, Dunigan DD (2023) The consumption of viruses returns energy to food chains. Proc Natl Acad Sci 120(1):e2215000120. https://doi.org/10.1073/pnas.2215000120
doi: 10.1073/pnas.2215000120
pubmed: 36574690
DeLong JP, Van Etten JL, Dunigan DD (2023) Lessons from chloroviruses: the complex and diverse roles of viruses in food webs. J Virol 0(0), e00275-23 https://doi.org/10.1128/jvi.00275-23
Dunigan DD, Al-Sammak M, Al-Ameeli Z, Agarkova IV, DeLong JP, Van Etten JL (2019) Chloroviruses lure hosts through long-distance chemical signaling. J Virol 93(7):e01688-e1718. https://doi.org/10.1128/JVI.01688-18
doi: 10.1128/JVI.01688-18
pubmed: 30626679
pmcid: 6430536
Engl T, Kaltenpoth M (2018) Influence of microbial symbionts on insect pheromones. Nat Prod Rep 35(5):386–397. https://doi.org/10.1039/C7NP00068E
doi: 10.1039/C7NP00068E
pubmed: 29565067
Hansson L (1997) Behavioural response in plants: adjustment in algal recruitment induced by herbivores. Proc R Soc London, Ser B 263(1374):1241–1244. https://doi.org/10.1098/rspb.1996.0182
doi: 10.1098/rspb.1996.0182
Kandasamy D, Gershenzon J, Andersson MN, Hammerbacher A (2019) Volatile organic compounds influence the interaction of the Eurasian spruce bark beetle (Ips typographus) with its fungal symbionts. ISME J 13(7):1788–1800. https://doi.org/10.1038/s41396-019-0390-3 . Article 7
doi: 10.1038/s41396-019-0390-3
pubmed: 30872804
pmcid: 6775991
Karakashian SJ (1963) Growth of Paramecium bursaria as influenced by the presence of algal symbionts. Physiol Zool 36(1):52–68. https://doi.org/10.1086/physzool.36.1.30152738
doi: 10.1086/physzool.36.1.30152738
Kavaliers M, Wiebe JP, Galea LAM (1994) Reduction of predator odor-induced anxiety in mice by the neurosteroid 3α-hydroxy-4-pregnen-20-one (3αHP). Brain Res 645(1):325–329. https://doi.org/10.1016/0006-8993(94)91667-5
doi: 10.1016/0006-8993(94)91667-5
pubmed: 7914815
Mathis A, Chivers DP, Smith RJF (1993) Population differences in responses of fathead minnows (Pimephales promelas) to visual and chemical stimuli from predators. Ethology 93(1):31–40. https://doi.org/10.1111/j.1439-0310.1993.tb00976.x
doi: 10.1111/j.1439-0310.1993.tb00976.x
O’halloran DM, Burnell AM (2003) An investigation of chemotaxis in the insect parasitic nematode Heterorhabditis bacteriophora. Parasitology 127(4):375–385. https://doi.org/10.1017/S0031182003003688
doi: 10.1017/S0031182003003688
pubmed: 14636024
Olive M, Moerman F, Fernandez-Cassi X, Altermatt F, Kohn T (2022) Removal of waterborne viruses by Tetrahymena pyriformis is virus-specific and coincides with changes in protist swimming speed. Environ Sci Technol 56(7):4062–4070. https://doi.org/10.1021/acs.est.1c05518
doi: 10.1021/acs.est.1c05518
pubmed: 35258957
pmcid: 8988290
Petri B, Sanz M-J (2018) Neutrophil chemotaxis. Cell Tissue Res 371(3):425–436. https://doi.org/10.1007/s00441-017-2776-8
doi: 10.1007/s00441-017-2776-8
pubmed: 29350282
Raina J-B, Fernandez V, Lambert B, Stocker R, Seymour JR (2019) The role of microbial motility and chemotaxis in symbiosis. Nat Rev Microbiol 17(5):284–294. https://doi.org/10.1038/s41579-019-0182-9 . Article 5
doi: 10.1038/s41579-019-0182-9
pubmed: 30923350
Reeder PB, Ache BW (1980) Chemotaxis in the Florida spiny lobster, Panulirus argus. Animal Behav 28(3):831–839. https://doi.org/10.1016/S0003-3472(80)80143-6
doi: 10.1016/S0003-3472(80)80143-6
Richard F-J, Poulsen M, Hefetz A, Errard C, Nash DR, Boomsma JJ (2007) The origin of the chemical profiles of fungal symbionts and their significance for nestmate recognition in Acromyrmex leaf-cutting ants. Behav Ecol Sociobiol 61(11):1637–1649. https://doi.org/10.1007/s00265-007-0395-1
doi: 10.1007/s00265-007-0395-1
Salsbery ME (2022) Evolutionary and ecological consequences of symbiosis in Paramecium bursaria [Ph.D., The University of Nebraska - Lincoln]. https://www.proquest.com/docview/2658283323/abstract/612CA1EEEE944738PQ/1
Salsbery ME, DeLong JP (2018) The benefit of algae endosymbionts in Paramecium bursaria is temperature dependent. Evol Ecol Res 19(6):669–678
Salsbery ME, DeLong JP (2021) Thermal adaptation in a holobiont accompanied by phenotypic changes in an endosymbiont. Evolution 75(8):2074–2084. https://doi.org/10.1111/evo.14301
doi: 10.1111/evo.14301
pubmed: 34192342
Shu L, Zhang B, Queller DC, Strassmann JE (2018) Burkholderia bacteria use chemotaxis to find social amoeba Dictyostelium discoideum hosts. ISME J 12(8):977–1993. https://doi.org/10.1038/s41396-018-0147-4 . Article 8
doi: 10.1038/s41396-018-0147-4
Stone CF, Moore J (2014) Parasite-induced alteration of odour responses in an amphipod–acanthocephalan system. Int J Parasitol 44(13):969–975. https://doi.org/10.1016/j.ijpara.2014.06.012
doi: 10.1016/j.ijpara.2014.06.012
pubmed: 25200352
Van Etten JL, Burbank DE, Kuczmarski D, Meints RH (1983) Virus infection of culturable chlorella-like algae and development of a plaque assay. Science 219(4587):994–996
doi: 10.1126/science.219.4587.994
pubmed: 17817937
Van Etten JL, Lane LC, Meints RH (1991) Viruses and virus-like particles of eukaryotic algae. Microbiol Rev 55(4):586–620. https://doi.org/10.1128/mr.55.4.586-620.1991
doi: 10.1128/mr.55.4.586-620.1991
pmcid: 372839
Wong-Ng J, Celani A, Vergassola M (2018) Exploring the function of bacterial chemotaxis. Curr Opin Microbiol 45:16–21. https://doi.org/10.1016/j.mib.2018.01.010
doi: 10.1016/j.mib.2018.01.010
pubmed: 29453124
Yashchenko VV, Gavrilova OV, Rautian MS, Jakobsen KS (2012) Association of Paramecium bursaria chlorella viruses with Paramecium bursaria cells: ultrastructural studies. Eur J Protistol 48(2):149–159. https://doi.org/10.1016/j.ejop.2011.05.002
doi: 10.1016/j.ejop.2011.05.002