Abstract
Although the response unit of living organisms to environmental changes is at the individual level, most experiments on the adaptation responses of ciliates have been conducted in batches, comprising multiple-individuals, due to their microscopic size. However, here, we confirmed that individuals undergo different division cycles in monocultures of Euplotes crassus. They also exhibited transcript variations of 4.63-fold in SSU and of 22.78- fold in Hsp70. Additionally, in salt-stressed E. crassus individuals, SSU transcripts of individuals varied by 6.92-fold at 27 psu, 8.69- fold at 32 psu, and 2.51-fold at 37 psu. However, the maximum difference in Hsp70 was only 4.23-fold under all conditions. These results suggest there may be different biological rhythms even in siblings derived from the same parent. It can also be inferred that various environmental factors have different effects on different E. crassus individuals. Therefore, to elucidate relationships between organism adaptations and environmental changes, studies at the individual level should be conducted with multi-individual approaches.
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Bahar R, Hartmann CH, Rodriguez KA, Denny AD, Busuttil RA, Dollé MET, Calder RB, Chisholm GB, Pollock BH, Klein CA (2006) Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 441:1011–1014
Becker AJ, Chen J, Paus S, Normann S, Beck H, Elger CE, Wiestler OD, Blümcke I (2002) Transcriptional profiling in human epilepsy: expression array and single cell real-time qRT-PCR analysis reveal distinct cellular gene regulation. Neuroreport 13:1327
Brandon RN (2014) Adaptation and environment. Princeton University Press, New Jersey, 228 p
Cohrs RJ, Randall J, Smith J, Gilden DH, Dabrowski C, Van Der Keyl H, Tal-Singer R (2000) Analysis of individual human trigeminal ganglia for latent herpes simplex virus type 1 and varicella-zoster virus nucleic acids using real-time PCR. J Virol 74:11464–11471
Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM (2011) Beyond predictions: biodiversity conservation in a changing climate. Science 332:53–58
Fenchel T (1987) Ecology of protozoa: the biology of free-living phagotrophic protists. Springer-Verlag, Heidelberg, 197 p
Foissner W (1991) Basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. Eur J Protistol 27:313–330
Halligan DL, Keightley PD (2009) Spontaneous mutation accumulation studies in evolutionary genetics. Annu Rev Ecol Syst 40:151–172
Hausmann K, Bradbury PC (1996) Ciliates: cells as organisms. Gustav Fischer Verlag, Heidelberg, 485 p
Herron MD (2016) Origins of multicellular complexity: Volvox and the volvocine algae. Mol Ecol 25:1213–1223
Huang X, Li Y, Zheng C (2009) A novel single-cell quantitative real-time RT-PCR method for quantifying foot-and-mouth disease viral RNA. J Virol Methods 155:150–156
Huang AG, Tu X, Liu L, Wang GX, Ling F (2016) The oxidative stress response of myclobutanil and cyproconazole on Tetrahymena thermophila. Environ Toxicol Phar 41:211–218
Jung JH, Kim S, Ryu S, Kim MS, Baek YS, Kim SJ, Choi JK, Park JK, Min GS (2012) Development of single-nucleotide polymorphismbased phylum-specific PCR amplification technique: application to the community analysis using ciliates as a reference organism. Mol Cells 34:383–391
Kasemets K, Ivask A, Dubourguier HC, Kahru A (2009) Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicol In Vitro 23:1116–1122
Kianianmomeni A, Hallmann A (2015) Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light-signaling pathways. Curr Genet 61:3–18
Kim SJ, Min GS (2009) Optimization of DNA extraction from a single living ciliate for stable and repetitive PCR amplification. Anim Cells Syst 13:351–356
Kim SJ, Choi JK, Ryu S, Min GS (2011) Single-cell PCR on protargol-impregnated euplotid ciliates: a combined approach of morphological and molecular taxonomy. Anim Cells Syst 15:251–258
Kim S, Kim SJ, Lee J, Lee YM (2014) Acute effects of heavy metals on the expression of glutathione-related antioxidant genes in the marine ciliate Euplotes crassus. Mar Pollut Bull 85:455–462
Kim YO, Shin K, Jang PG, Choi HW, Noh JH, Yang EJ, Kim E, Jeon D (2012) Tintinnid species as biological indicators for monitoring intrusion of the warm oceanic waters into Korean coastal waters. Ocean Sci J 47:161–172
Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of Cope's rule of phyletic size increase. Evolution 58:1608–1612
Koch F, Kang Y, Villareal TA, Anderson DM, Gobler CJ (2014) A novel immunofluorescence flow cytometry technique detects the expansion of brown tides caused by Aureoumbra lagunensis to the Caribbean Sea. Appl Environ Microb 80:4947–4957
Kvitek L, Vanickova M, Panacek A, Soukupova J, Dittrich M, Valentova E, Prucek R, Bancirova M, Milde D, Zboril R (2009) Initial study on the toxicity of silver nanoparticles (NPs) against Paramecium caudatum. J Phys Chem C 113:4296–4300
Lamichhaney S, Berglund J, Almén MS, Maqbool K, Grabherr M, Martinez-Barrio A, Promerova´ M, Rubin CJ, Wang C, Zamani N, Grant BR, Grant PR, Webster MT, Andersson L (2015) Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518:371–375
Lampert T, Nugent C, Weston J, Braun N, Kuruvilla H (2013) Nociceptin signaling involves a calcium-based depolarization in Tetrahymena thermophila. Int J Pept 2013:573716. doi: 10.1155/2013/573716
Liss B (2002) Improved quantitative real-time RT–PCR for expression profiling of individual cells. Nucleic Acids Res 30:e89. doi: 10.1093/nar/gnf088
Li J, Zhou L, Lin X, Yi Z, Khaled ASAl-R (2014) Characterizing dose–responses of catalase to nitrofurazone exposure in model ciliated protozoan Euplotes vannus for ecotoxicity assessment: Enzyme activity and mRNA expression. Ecotox Environ Safe 100:294–302
Lynn DH (2008) The ciliated protozoa: characterization, classification, and guide to the literature. Springer Science & Business Media, Heidelberg, 605 p
McGee MD, Borstein SR, Neches RY, Buescher HH, Seehausen OW, Peter C (2015) A pharyngeal jaw evolutionary innovation facilitated extinction in Lake Victoria cichlids. Science 350: 1077–1079
Martin PR, McKay JK, Noor M (2004) Latitudinal variation in genetic divergence of populations and the potential for future speciation. Evolution 58:938–945
Mayer M, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684
Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 10:315–331
Xu H, Song W, Warren A (2004) An investigation of the tolerance to ammonia of the marine ciliate Euplotes vannus (Protozoa, Ciliophora). Hydrobiologia 519:189–195
Newell RC (2013) Adaptation to environment: essays on the physiology of marine animals. Elsevier, Pennsylvania, 554 p
Nowacki M, Vijayan V, Zhou Y, Schotanus K, Doak TG, Landweber LF (2008) RNA-mediated epigenetic programming of a genomerearrangement pathway. Nature 451:153–158
Orr PT, Rasmussen JP, Burford MA, Eaglesham GK, Lennox SM (2010) Evaluation of quantitative real-time PCR to characterise spatial and temporal variations in cyanobacteria, Cylindrospermopsis raciborskii (Woloszynska) Seenaya et Subba Raju and cylindrospermopsin concentrations in three subtropical Australian reservoirs. Harmful Algae 9:243–254
Plough LV, Shin G, Hedgecock D (2016) Genetic inviability is a major driver of type III survivorship in experimental families of a highly fecund marine bivalve. Mol Ecol 25:895–910
Raikov IB (1969) The macronucleus of ciliates. In: Chen TT (ed) Research in protozoology. Pergamon Press, London, pp 1–128
Rantala-Ylinen A, Sipari H, Sivonen K (2011) Molecular methods: chip assay and quantitative real-time PCR: in detecting hepatotoxic cyanobacteria. Methods Mol Biol 739:73–86
Rasmussen R (2001) Quantification on the lightcycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR. Springer Press, Heidelberg, pp 21–34
Seyfert HM, Hipke H, Schmidt W (1984) Isolation and phenotypic characterization of Tetrahymena thermophila size mutants: the relationship between cell size and regulation of DNA content. J Cell Sci 67:203–215
Smith CJ, Osborn AM (2009) Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiol Ecol 67:6–20
Terza AL, Papa G, Miceli C, Luporini P (2001) Divergence between two Antarctic species of the ciliate Euplotes, E. focardii and E. nobilii, in the expression of heat-shock protein 70 genes. Mol Ecol 10:1061–1067
Trenfield MA, Ng JC, Noller B, Markich SJ, van Dam RA (2012) Dissolved organic carbon reduces uranium toxicity to the unicellular eukaryote Euglena gracilis. Ecotoxicology 21:1013–1023
Treutlein B, Lee QY, Camp JG, Mall M, Koh W, Shariati SAM, Sim S, Neff NF, Skotheim JM, Wernig M, Quake SR (2016) Dissecting direct reprogramming from fibroblast to neuron using single-cell RNA-seq. Nature 534:391–395
Veselenak RL, Miller AL, Milligan GN, Bourne N, Pyles RB (2015) Development and utilization of a custom PCR array workflow: analysis of gene expression in Mycoplasma genitalium and guinea pig (Cavia porcellus). Mol Biotechnol 57:172–183
Wacker M, Godard M (2005) Analysis of one-step and two-step real-time RT-PCR using SuperScript III. J Biomol Tech 16:266–271
Wallbank RWR, Baxter SW, Pardo-Diaz C, Hanly JJ, Martin SH, Mallet J, Dasmahapatra KK, Salazar C, Joron M, Nadeau N, McMillan WO, Jiggins CD (2016) Evolutionary novelty in a butterfly wing pattern through Enhancer shuffling. PLoS Biol 14:e1002353. doi:10.1371/journal.pbio.1002353
Xu H, Song W, Warren A (2004) An investigation of the tolerance to ammonia of the marine ciliate Euplotes vannus (Protozoa, Ciliophora). Hydrobiologia 519:189–195
Zufall RA, Dimond KL, Doerder FD (2013) Restricted distribution and limited gene flow in the model ciliate Tetrahymena thermophila. Mol Ecol 22:1081–1091
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Kim, SJ., Kim, JH. & Ju, SJ. Adaptation responses of individuals to environmental changes in the ciliate Euplotes crassus . Ocean Sci. J. 52, 127–138 (2017). https://doi.org/10.1007/s12601-017-0014-7
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DOI: https://doi.org/10.1007/s12601-017-0014-7