Growth response of the ichthyotoxic haptophyte, Prymnesium parvum Carter, to changes in sulfate and fluoride concentrations
Autoři:
Rakib H. Rashel aff001; Reynaldo Patiño aff002
Působiště autorů:
Department of Biological Sciences and Texas Cooperative Fish and Wildlife Research Unit, Texas Tech University, Lubbock, Texas, United States of America
aff001; U.S. Geological Survey, Texas Cooperative Fish and Wildlife Research Unit and Departments of Natural Resources Management and Biological Sciences, Texas Tech University, Lubbock, Texas, United States of America
aff002
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223266
Souhrn
Golden alga Prymnesium parvum Carter is a euryhaline, ichthyotoxic haptophyte (Chromista). Because of its presumed coastal/marine origin where SO42- levels are high, the relatively high SO42- concentration of its brackish inland habitats, and the sensitivity of marine chromists to sulfur deficiency, this study examined whether golden alga growth is sensitive to SO42- concentration. Fluoride is a ubiquitous ion that has been reported at higher levels in golden alga habitat; thus, the influence of F- on growth also was examined. In low-salinity (5 psu) artificial seawater medium, overall growth was SO42—dependent up to 1000 mg l-1 using MgSO4 or Na2SO4 as source; the influence on growth rate, however, was more evident with MgSO4. Transfer from 5 to 30 psu inhibited growth when salinity was raised with NaCl but in the presence of seawater levels of SO42-, these effects were fully reversed with MgSO4 as source and only partially reversed with Na2SO4. Growth inhibition was not observed after acute transfer to 30 psu in a commercial sea salt mixture. In 5-psu medium, F- inhibited growth at all concentrations tested. These observations support the hypothesis that spatial differences in SO42- –but not F-–concentration help drive the inland distribution and growth of golden alga and also provide physiological relevance to reports of relatively high Mg2+ concentrations in golden alga habitat. At high salinity, however, the ability of sulfate to maintain growth under osmotic stress was weak and overshadowed by the importance of Mg2+. A mechanistic understanding of growth responses of golden alga to SO42-, Mg2+ and other ions at environmentally relevant levels and under different salinity scenarios will be necessary to clarify their ecophysiological and evolutionary relevance.
Klíčová slova:
Sulfates – Algae – Osmotic shock – Fluorides – Salinity – Sea water – Fresh water – Surface water
Zdroje
1. Nicholls KH. Haptophyte Algae. In: Wehr JD, Sheath RG, editors. Freshwater Algae of North America. Boston: Academic Press; 2003. pp. 511–521.
2. Edvardsen B, Imai I. The Ecology of Harmful Flagellates Within Prymnesiophyceae and Raphidophyceae. In: Granéli E, Turner JT, editors. Ecology of Harmful Algae. Berlin, Heidelberg: Springer; 2006. pp. 67–79.
3. Roelke DL, Barkoh A, Brooks BW, Grover JP, Hambright KD, La Claire JW Ⅱ., et al. A chronicle of a killer alga in the west: ecology, assessment, and management of Prymnesium parvum blooms. Hydrobiologia. 2016;764(1): 29–50.
4. Israël NMD, VanLandeghem MM, Denny S, Ingle J, Patiño R. Golden alga presence and abundance are inversely related to salinity in a high-salinity river ecosystem, Pecos River, USA. Harmful Algae. 2014;39: 81–91.
5. Weimin G. The reason for the fish death at aquacultural experimental station at Ningxia and the distribution of Prymnesium parvum in Ningxia. Jouranl Dalian Fish Coll. 1983;1: 43–48 (in Chinese).
6. Guo M, Harrison PJ, Taylor FJR. Fish kills related to Prymnesium parvum N. Carter (Haptophyta) in the People’s Republic of China. J Appl Phycol. 1996;8(2): 111–117.
7. Rashel RH, Patiño R. Influence of genetic background, salinity, and inoculum size on growth of the ichthyotoxic golden alga (Prymnesium parvum). Harmful Algae. 2017;66: 97–104. doi: 10.1016/j.hal.2017.05.010 28602258
8. Hambright KD, Zamor RM, Easton JD, Glenn KL, Remmel EJ, Easton AC. Temporal and spatial variability of an invasive toxigenic protist in a North American subtropical reservoir. Harmful Algae. 2010;9(6): 568–577.
9. Granéli E, Edvardsen B, Roelke DL, Hagström JA. The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae. 2012;14: 260–270.
10. Roelke DL, Brooks BW, Grover JP, Gable GM, Schwierzke-Wade L, Hewitt NC, et al. Anticipated human population and climate change effects on algal blooms of a toxic haptophyte in the south-central USA. Can J Fish Aquat Sci. 2012;69(8):1389–1404.
11. Patiño R, Dawson D, VanLandeghem MM. Retrospective analysis of associations between water quality and toxic blooms of golden alga (Prymnesium parvum) in Texas reservoirs: Implications for understanding dispersal mechanisms and impacts of climate change. Harmful Algae. 2014;33: 1–11.
12. VanLandeghem MM, Farooqi M, Southard GM, Patiño R. Associations between Water Physicochemistry and Prymnesium parvum Presence, Abundance, and Toxicity in West Texas Reservoirs. J Am Water Resour Assoc. 2015;51(2): 471–486.
13. Vanlandeghem MM, Farooqi M, Southard GM, Patiño R. Spatiotemporal associations of reservoir nutrient characteristics and the invasive, harmful alga Prymnesium parvum in West Texas. J Am Water Resour Assoc. 2015;51(2): 487–501.
14. Dillon PJ, Kirchner WB. The effects of geology and land use on the export of phosphorus from watersheds. Water Res. 1975;9(2): 135–148.
15. Foley JA, Defries R, Asner GP, Barford C, Bonan G, Carpenter SR, et al. Global consequences of land use. Science. 2005;309(5734): 570–574. doi: 10.1126/science.1111772 16040698
16. Kaushal SS, Groffman PM, Likens GE, Belt KT, Stack WP, Kelly VR, et al. Increased salinization of fresh water in the northeastern United States. Proc Natl Acad Sci USA. 2005;102(38): 13517–13520. doi: 10.1073/pnas.0506414102 16157871
17. VanLandeghem MM, Meyer MD, Cox SB, Sharma B, Patiño R. Spatial and temporal patterns of surface water quality and ichthyotoxicity in urban and rural river basins in Texas. Water Res. 2012;46(20): 6638–6651. doi: 10.1016/j.watres.2012.05.002 22682267
18. Moestrup Ø. Economic aspects: ‘blooms’, nuisance species and toxins. In: Green JC, Leadbeater BSC, editors. The Haptophyte Algae. Oxford: Clarendon Press; 1994. pp. 265–285.
19. Takahashi H, Kopriva S, Giordano M, Saito K, Hell R. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol. 2011;62(1): 157–184.
20. Giordano M, Raven JA. Nitrogen and sulfur assimilation in plants and algae. Aquat Bot. 2014;118: 45–61.
21. Holmer M, Storkholm P. Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw Biol. 2001;46(4): 431–451.
22. Prioretti L, Giordano M. Direct and indirect influence of sulfur availability on phytoplankton evolutionary trajectories. J Phycol. 2016;52(6): 1094–1102. doi: 10.1111/jpy.12468 27716928
23. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, et al. The evolution of modern eukaryotic phytoplankton. Science. 2004;305(5682): 354–360. doi: 10.1126/science.1095964 15256663
24. Cavalier-Smith T. Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences. Protoplasma. 2018;255(1): 297–357. doi: 10.1007/s00709-017-1147-3 28875267
25. Yildiz FH, Davies JP, Grossman AR. Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol. 1994;104(3): 981–987. doi: 10.1104/pp.104.3.981 12232142
26. Giordano M, Norici A, Hell R. Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol. 2005;166(2): 371–382. doi: 10.1111/j.1469-8137.2005.01335.x 15819903
27. Ratti S, Knoll AH, Giordano M. Did sulfate availability facilitate the evolutionary expansion of chlorophyll a+c phytoplankton in the oceans? Geobiology. 2011;9(4): 301–312. doi: 10.1111/j.1472-4669.2011.00284.x 21627761
28. Bochenek M, Etherington GJ, Koprivova A, Mugford ST, Bell TG, Malin G, et al. Transcriptome analysis of the sulfate deficiency response in the marine microalga Emiliania huxleyi. New Phytol. 2013;199(3): 650–662. doi: 10.1111/nph.12303 23692606
29. Dobbs C.G. Fluoride and the environment. Fluoride. 1974;7(3): 123–135.
30. Camargo JA. Estimating safe concentrations of fluoride for three species of nearctic freshwater invertebrates: Multifactor Probit Analysis. Bull Environ Contam Toxicol. 1996;56(4): 643–648. doi: 10.1007/s001289900094 8645924
31. Camargo JA. Fluoride toxicity to aquatic organisms: a review. Chemosphere. 2003;50(3): 251–264. doi: 10.1016/s0045-6535(02)00498-8 12656244
32. Lutz-Carrillo DJ, Southard GM, Fries LT. Global genetic relationships among isolates of golden alga (Prymnesium parvum). J Am Water Resour Assoc. 2010;46(1): 24–32.
33. Finkle BJ, Appleman D. The effect of magnesium concentration on growth of Chlorella. Plant Physiol. 1953;28(4): 664–673. doi: 10.1104/pp.28.4.664 16654583
34. Atkinson MJ, Bingman C. Elemental composition of commercial seasalts. J Aquaric Aquat Sci. 1998;8(2): 39–43.
35. Wood AM, Everroad RC, Wingard L. Measuring growth rates in microalgal cultures. In: Andersen RA., editor. Algal Culturing Techniques. Elsevier Academic Press; 2005. p. 598.
36. Holm S. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics. 1979;6 (2): 65–70.
37. Padilla GM. Growth and toxigenesis of the chrysomonad Prymnesium parvum as a function of salinity. The Journal of Protozoology. 1970;177: 456–462.
38. Larsen A, Bryant S. Growth rate and toxicity of Prymnesium parvum and Prymnesium patelliferum (Haptophyta) in response to changes in salinity, light and temperature. Sarsia. 1998;83(5): 409–418.
39. Baker JW, Grover JP, Brooks BW, Ureña-Boeck F, Roelke DL, Errera R, et al. Growth and toxicity of Prymnesium parvum (Haptophyta) as a function of salinity, light, and temperature. J Phycol. 2007;43(2): 219–227.
40. Hambright KD, Easton JD, Zamor RM, Beyer J, Easton AC, Allison B. Regulation of growth and toxicity of a mixotrophic microbe: implications for understanding range expansion in Prymnesium parvum. Freshw Sci. 2014;33(3): 745–754.
41. Hilt KL, Gordon PR, Hein A, Caulfield JP, Falchuk KH. Effects of Iron-, Manganese-, or Magnesium-deficiency on the growth and morphology of Euglena gracilis. J Protozool. 1987;34(2): 192–198. doi: 10.1111/j.1550-7408.1987.tb03159.x 3108492
42. Weiss M, Haimovich G, Pick U. Phosphate and sulfate uptake in the halotolerant alga Dunaliella are driven by Na+-symport mechanism. J Plant Physiol. 2001;158(12): 1519–1525.
43. Esakkimuthu S, Krishnamurthy V, Govindarajan R, Swaminathan K. Augmentation and starvation of calcium, magnesium, phosphate on lipid production of Scenedesmus obliquus. Biomass and Bioenergy. 2016;88: 126–134.
44. Srivastava G, Nishchal, Goud VV. Salinity induced lipid production in microalgae and cluster analysis (ICCB 16-BR_047). Bioresource Technology. 2017;242: 244–252. doi: 10.1016/j.biortech.2017.03.175 28390788
45. Talarski A, Manning SR, La Claire JW Ⅱ. Transcriptome analysis of the euryhaline alga, Prymnesium parvum (Prymnesiophyceae): effects of salinity on differential gene expression. Phycologia. 2016;55(1): 33–44.
46. Kobayashi NI, Tanoi K. Critical issues in the study of magnesium transport systems and magnesium deficiency symptoms in plants. Int J Mol Sci. 2015;16(9): 23076–23093. doi: 10.3390/ijms160923076 26404266
47. Igamberdiev AU, Kleczkowski LA. Magnesium and cell energetics in plants under anoxia. Biochem J. 2011;437(3): 373–379. doi: 10.1042/BJ20110213 21749322
48. Ochoa-Herrera V, Banihani Q, León G, Khatri C, Field JA, Sierra-Alvarez R. Toxicity of fluoride to microorganisms in biological wastewater treatment systems. Water Res. 2009;43(13): 3177–3186. doi: 10.1016/j.watres.2009.04.032 19457531
49. Hekman WE, Budd K, Palmer GR, MacArthur JD. Responses of certain freshwater planktonic algae to fluoride. J Phycol. 1984;20(2): 243–249.
50. Bhatnagar M, Bhatnagar A. Algal and cyanobacterial responses to fluoride. Fluoride. 2000;33(2): 55–65.
51. Wu Y, Li P, Zhao X. Effect of fluoride on carbonic anhydrase activity and photosynthetic oxygen evolution of the algae Chlamydomonas reinhardtii. Fluoride. 2007;40(1): 51–64.
52. Norici A, Hell R, Giordano M. Sulfur and primary production in aquatic environments: an ecological perspective. Photosynth Res. 2005;86(3): 409–417. doi: 10.1007/s11120-005-3250-0 16307310
53. Chen L, Gin KYH, He Y. Effects of sulfate on microcystin production, photosynthesis, and oxidative stress in Microcystis aeruginosa. Environ Sci Pollut Res. 2016;23(4): 3586–3595.
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Je Fuchsova endotelová dystrofie rohovky neurodegenerativní onemocnění?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania