Strong and widespread cycloheximide resistance in Stichococcus-like eukaryotic algal taxa.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 01 2022
20 01 2022
Historique:
received:
05
04
2021
accepted:
04
01
2022
entrez:
21
1
2022
pubmed:
22
1
2022
medline:
3
3
2022
Statut:
epublish
Résumé
This study was initiated following the serendipitous discovery of a unialgal culture of a Stichococcus-like green alga (Chlorophyta) newly isolated from soil collected on Signy Island (maritime Antarctica) in growth medium supplemented with 100 µg/mL cycloheximide (CHX, a widely used antibiotic active against most eukaryotes). In order to test the generality of CHX resistance in taxa originally identified as members of Stichococcus (the detailed taxonomic relationships within this group of algae have been updated since our study took place), six strains were studied: two strains isolated from recent substrate collections from Signy Island (maritime Antarctica) ("Antarctica" 1 and "Antarctica" 2), one isolated from this island about 50 years ago ("Antarctica" 3) and single Arctic ("Arctic"), temperate ("Temperate") and tropical ("Tropical") strains. The sensitivity of each strain towards CHX was compared by determining the minimum inhibitory concentration (MIC), and growth rate and lag time when exposed to different CHX concentrations. All strains except "Temperate" were highly resistant to CHX (MIC > 1000 µg/mL), while "Temperate" was resistant to 62.5 µg/mL (a concentration still considerably greater than any previously reported for algae). All highly resistant strains showed no significant differences in growth rate between control and treatment (1000 µg/mL CHX) conditions. Morphological examination suggested that four strains were consistent with the description of the species Stichococcus bacillaris while the remaining two conformed to S. mirabilis. However, based on sequence analyses and the recently available phylogeny, only one strain, "Temperate", was confirmed to be S. bacillaris, while "Tropical" represents the newly erected genus Tetratostichococcus, "Antarctica 1" Tritostichococcus, and "Antarctica 2", "Antarctica 3" and "Arctic" Deuterostichococcus. Both phylogenetic and CHX sensitivity analyses suggest that CHX resistance is potentially widespread within this group of algae.
Identifiants
pubmed: 35058560
doi: 10.1038/s41598-022-05116-y
pii: 10.1038/s41598-022-05116-y
pmc: PMC8776791
doi:
Substances chimiques
DNA, Algal
0
Soil
0
Cycloheximide
98600C0908
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1080Subventions
Organisme : YPASM
ID : 304/PBIOLOGI/650963
Organisme : RUI
ID : 1001/PBIOLOGI/811305
Informations de copyright
© 2022. The Author(s).
Références
D’Costa, V. M. et al. Antibiotic resistance is ancient. Nature 477, 457–461 (2011).
pubmed: 21881561
doi: 10.1038/nature10388
Kaur, P. & Peterson, E. Antibiotic resistance mechanisms in bacteria: Relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Front. Microbiol. 9, 2928 (2018).
pubmed: 30555448
pmcid: 6283892
doi: 10.3389/fmicb.2018.02928
Munita, J. M. & Arias, C. A. Mechanisms of antibiotic resistance. Microbiol. Spectr. 4, 1–24 (2016).
doi: 10.1128/microbiolspec.VMBF-0016-2015
Leach, B. E., Ford, J. H. & Whiffen, A. J. Actidione, an antibiotic from Streptomyces griseus. J. Am. Chem. Soc. 69, 474 (1947).
pubmed: 20292455
doi: 10.1021/ja01194a519
Schneider-Poetsch, T. et al. Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 6, 209–217 (2010).
pubmed: 20118940
pmcid: 2831214
doi: 10.1038/nchembio.304
Whiffen, A. J. The production, assay, and antibiotic activity of actidione, an antibiotic from Streptomyces griseus. J. Bacteriol. 56, 283 (1948).
pubmed: 18880569
pmcid: 518581
doi: 10.1128/jb.56.3.283-291.1948
Palmer, C. M. & Maloney, T. E. Preliminary screening for potential algicides. Ohio J. Sci. 55, 1–8 (1955).
Zehnder, A. & Hughes, E. O. The antialgal activity of actidione. Can. J. Microbiol. 4, 399–408 (1958).
pubmed: 13561191
doi: 10.1139/m58-042
Hunter, E. O. Jr. & McVeigh, I. The effects of selected antibiotics on pure cultures of algae. Am. J. Bot. 48, 179–185 (1961).
doi: 10.1002/j.1537-2197.1961.tb11623.x
Vaara, T., Vaara, M. & Niemelä, S. Two improved methods for obtaining axenic cultures of cyanobacteria. Appl. Environ. Microbiol. 38, 1011–1014 (1979).
pubmed: 16345455
pmcid: 243622
doi: 10.1128/aem.38.5.1011-1014.1979
Castenholz, R. W. Culturing methods for cyanobacteria. Methods Enzymol. 167, 68–93 (1988).
doi: 10.1016/0076-6879(88)67006-6
Bolch, C. J. & Blackburn, S. I. Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kützing. J. Appl. Phychol. 8, 5–13 (1996).
doi: 10.1007/BF02186215
Choi, G. G., Bae, M. S., Ahn, C. Y. & Oh, H. M. Induction of axenic culture of Arthrospira (Spirulina) platensis based on antibiotic sensitivity of contaminating bacteria. Biotechnol. Lett. 30, 87–92 (2008).
pubmed: 17846705
doi: 10.1007/s10529-007-9523-2
Katoh, H., Furukawa, J., Tomita-Yokotani, K. & Nishi, Y. Isolation and purification of an axenic diazotrophic drought-tolerant cyanobacterium, Nostoc commune, from natural cyanobacterial crusts and its utilization for field research on soils polluted with radioisotopes. Biochim. Biophys. Acta. 1817, 1499–1505 (2008).
doi: 10.1016/j.bbabio.2012.02.039
Mutoh, E., Ohta, A. & Takagi, M. Studies on cycloheximide-sensitive and cycloheximide-resistant ribosomes in the yeast Candida maltosa. Gene 224, 9–15 (1998).
pubmed: 9931408
doi: 10.1016/S0378-1119(98)00518-6
Takagi, M., Kawai, S., Shibuya, I., Miyazaki, M. & Yano, K. Cloning in Saccharomyces cerevisiae of a cycloheximide resistance gene from the Candida maltosa genome which modifies ribosomes. J. Bacteriol. 68, 417–419 (1986).
doi: 10.1128/jb.168.1.417-419.1986
Dehoux, P., Davies, J. & Cannon, M. Natural cycloheximide resistance in yeast: The role of ribosomal protein L41. Eur. J. Biochem. 213, 841–848 (1993).
pubmed: 8477753
doi: 10.1111/j.1432-1033.1993.tb17827.x
Adoutte-Panvier, A. & Davies, J. E. Studies of ribosomes of yeast species: Susceptibility to inhibitors of protein synthesis in vivo and in vitro. Mol. Gen. Genet. 194, 310–317 (1984).
doi: 10.1007/BF00383533
Yagisawa, F. et al. Isolation of cycloheximide-resistant mutants of Cyanidioschyzon merolae. Cytologia 69, 97–100 (2004).
doi: 10.1508/cytologia.69.97
Thomas, D. N. et al. The Biology of Polar Regions 2nd edn. (Oxford University Press, 2008).
doi: 10.1093/acprof:oso/9780199298112.001.0001
Hughes, K. A. Solar UV-B radiation, associated with ozone depletion, inhibits the Antarctic terrestrial microalga, Stichococcus bacillaris. Polar Biol. 29, 327–336 (2006).
doi: 10.1007/s00300-005-0057-6
Karsten, U. & Holzinger, A. Green algae in alpine biological soil crust communities: Acclimation strategies against ultraviolet radiation and dehydration. Biodivers. Conserv. 23, 1845–1858 (2014).
pubmed: 24954980
pmcid: 4058318
doi: 10.1007/s10531-014-0653-2
Shekh, R. M., Singh, P., Singh, S. M. & Roy, U. Antifungal activity of Arctic and Antarctic bacteria isolates. Polar Biol. 34, 139–143 (2011).
doi: 10.1007/s00300-010-0854-4
Wiser, M. J. & Lenski, R. E. A comparison of methods to measure fitness in Escherichia coli. PLoS ONE 10, 10 (2015).
doi: 10.1371/journal.pone.0126210
Fritsch, F. E. The Structure and Reproduction of the Algae Vol. II (Cambridge University Press, 1959).
Fukushima, H. Studies on cryophytes in Japan. J. Yokohama Munic Univ. Ser. C 43, 1–146 (1963).
Hoham, R. W. Pleiomorphism in the snow alga, Raphidonema nivale Lagerh (Chlorophyta), and a revision of the genus Raphidonema Lagerh. Syesis 6, 255–263 (1973).
Pröschold, T. & Darienko, T. The green puzzle Stichococcus (Trebouxiophyceae, Chlorophyta): New generic and species concept among this widely distributed genus. Phytotaxa 2, 113–142 (2020).
doi: 10.11646/phytotaxa.441.2.2
Hodač, L. et al. Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol. Ecol. 92, 1–16 (2016).
doi: 10.1093/femsec/fiw122
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: 27th Informational Supplement (Clinical and Laboratory Standards Institute, 2017).
European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). EUCAST discussion document E.Dis. 5.1. Determination of minimum inhibitory concentrations (MIC’s) of antibacterial agents by broth dilution. Clin. Microbiol. Infect. 9, 1–7 (2003).
Bertrand, R. L. Lag phase is a dynamic, organized, adaptive, and evolvable period that prepares bacteria for cell division. J. Bacteriol. 201, e00697-e718 (2019).
pubmed: 30642990
pmcid: 6416914
doi: 10.1128/JB.00697-18
Claesson, A. & Törnqvist, L. The toxicity of aluminium to two acido-tolerant green algae. Water Res. 22, 977–983 (1988).
doi: 10.1016/0043-1354(88)90144-3
Knapp, C. W. et al. Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS ONE 6, e27300 (2011).
pubmed: 22096547
pmcid: 3212566
doi: 10.1371/journal.pone.0027300
Su, J. Q., Wei, B., Xu, C. Y., Qiao, M. & Zhu, Y. G. Functional metagenomic characterization of antibiotic resistance genes in agricultural soils from China. Environ. Int. 65, 9–15 (2014).
pubmed: 24412260
doi: 10.1016/j.envint.2013.12.010
Tomova, I., Stoilova-Disheva, M., Lazarkevich, I. & Vasileva-Tonkova, E. Antibiotic activity and resistance to heavy metals and antibiotics of heterotrophic bacteria isolated from sediment and soil samples collected from two Antarctic islands. Front. Life Sci. 8, 348–357 (2015).
doi: 10.1080/21553769.2015.1044130
Van Goethem, M. W. et al. A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils. Microbiome 6, 40 (2018).
pubmed: 29471872
pmcid: 5824556
doi: 10.1186/s40168-018-0424-5
Cowan, D. A. et al. Non-indigenous microorganisms in the Antarctic: Assessing the risks. Trends Microbiol. 19, 540–548 (2011).
pubmed: 21893414
doi: 10.1016/j.tim.2011.07.008
Convey, P. et al. The spatial structure of Antarctic biodiversity. Ecol. Monogr. 84, 203–244 (2014).
doi: 10.1890/12-2216.1
Cowan, D. A., Makhalanyane, T. P., Dennis, P. G. & Hopkins, D. W. Microbial ecology and biogeochemistry of continental Antarctic soils. Front. Microbiol. 5, 154 (2014).
pubmed: 24782842
pmcid: 3988359
doi: 10.3389/fmicb.2014.00154
Lo Giudice, A., Bruni, V. & Michaud, L. Characterization of Antarctic psychrotrophic bacteria with antibacterial activities against terrestrial microorganisms. J. Basic Microbiol. 47, 496–505 (2007).
pubmed: 18072250
doi: 10.1002/jobm.200700227
Bell, T., Callender, K., Whyte, L. & Greer, C. Microbial competition in polar soils: A review of an understudied but potentially important control on productivity. Biology 2, 533–554 (2013).
pubmed: 24832797
pmcid: 3960893
doi: 10.3390/biology2020533
Núñez-Montero, K. & Barrientos, L. Advances in Antarctic research for antibiotic discovery: A comprehensive narrative review of bacteria from Antarctic environments as potential sources of novel antibiotic compounds against human pathogens and microorganisms of industrial importance. Antibiotics 7, 90 (2018).
pmcid: 6316688
doi: 10.3390/antibiotics7040090
Davies, J. Are antibiotics naturally antibiotics?. J. Ind. Microbiol. Biotechnol. 33, 496–499 (2006).
pubmed: 16552582
doi: 10.1007/s10295-006-0112-5
Levy, S. B. Antibiotic resistance: Consequences of inaction. Clin. Infect. Dis. 33, 124–129 (2001).
doi: 10.1086/321837
Marshall, B. M. & Levy, S. B. Food animals and antimicrobials: Impacts on human health. Clin. Microbiol. Rev. 24, 718–733 (2011).
pubmed: 21976606
pmcid: 3194830
doi: 10.1128/CMR.00002-11
Andersson, D. I. & Hughes, D. Evolution of antibiotic resistance at non-lethal drug concentrations. Drug Resist. Updates 15, 162–172 (2012).
doi: 10.1016/j.drup.2012.03.005
Kuwabara, J. S. & Leland, H. V. Adaptation of Selenastrum capricornutum (Chlorophyceae) to copper. Environ. Toxicol. Chem. 5, 197–203 (1986).
doi: 10.1002/etc.5620050211
Martínez, J. L., Coque, T. M. & Baquero, F. What is a resistance gene? Ranking risk in resistomes. Nat. Rev. Microbiol. 13, 116 (2015).
pubmed: 25534811
doi: 10.1038/nrmicro3399
Bold, H. C. The morphology of Chlamydomonas chlamydogama sp. nov. Bull. Torrey Bot. Club 76, 101–108 (1949).
doi: 10.2307/2482218
Bischoff, H. & Bold, H. C. Phycological studies IV. Some soil algae from enchanted rock and related algal species. Univ. Texas Publ. 6318, 95 (1963).
Balouiri, M., Sadiki, M. & Ibnsouda, S. K. Methods for in vitro evaluating antibiotic activity: A review. J. Pharm. Anal. 6, 71–79 (2016).
pubmed: 29403965
doi: 10.1016/j.jpha.2015.11.005
Zhao, Q. et al. Microalgal microscale model for microalgal growth inhibition evaluation of marine natural products. Sci. Rep. 8, 10541 (2018).
pubmed: 30002474
pmcid: 6043507
doi: 10.1038/s41598-018-28980-z
LeGresley, M. & McDermott, G. Counting chamber methods for quantitative phytoplankton analysis—Haemocytometer, Palmer-Maloney cell and Sedgewick-Rafter cell. In Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis (eds Karlson, B. et al.) 25–30 (IOC Manuals and Guides. Intergovernmental Oceanographic Commission of UNESCO, 2010).
Hall, B. G., Acar, H., Nandipati, A. & Barlow, M. Growth rates made easy. Mol. Biol. Evol. 31, 232–238 (2010).
doi: 10.1093/molbev/mst187
Mattox, K. R. & Bold, H. C. Phycological studies III. The taxonomy of certain ulotrichacean algae. Univ. Texas Publ. 6222, 1–67 (1962).
Prescott, G. W. Algae of the Western Great Lakes area (C Bron Company Publishers, 2010).
John, D. M., Whitton, B. A. & Brook, A. J. The Freshwater Algal Flora of the British Isles 2nd edn. (Cambridge University Press, 2011).
Hallmann, C. et al. Molecular diversity of phototrophic biofilms on building stone. FEMS Microbiol. Ecol. 84, 355–372 (2013).
pubmed: 23278436
doi: 10.1111/1574-6941.12065
Liu, J., Gerken, H. & Li, Y. Single-tube colony PCR for DNA amplification and transformant screening of oleaginous microalgae. J. Appl. Phycol. 26, 1719–1726 (2014).
doi: 10.1007/s10811-013-0220-3
Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
pubmed: 9254694
pmcid: 146917
doi: 10.1093/nar/25.17.3389
Kanehisa, M., Goto, S., Sato, Y., Furumichi, M. & Tanabe, M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109–D114 (2011).
pubmed: 22080510
pmcid: 3245020
doi: 10.1093/nar/gkr988
Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).
pubmed: 16928733
doi: 10.1093/bioinformatics/btl446
Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).
pubmed: 12912839
doi: 10.1093/bioinformatics/btg180
Rambaut, A. FigTree. Version 1.3.1 [software]. Available from: http://www.treebioedacuk/software/figtree (2009).