Growth at the limits: comparing trace metal limitation of a freshwater cyanobacterium (Dolichospermum lemmermannii) and a freshwater diatom (Fragilaria crotonensis)
1.Galloway, J. N. et al. Trace metals in atmospheric deposition: A review and assessment. Atmos. Environ. 16, 1677–1700 (1982).CAS
ADS
Google Scholar
2.Dodds, W. K., Perkin, J. S. & Gerken, J. E. Human impact on freshwater ecosystem services: A global perspective. Environ. Sci. Technol. 47, 9061–9068 (2013).CAS
PubMed
ADS
Google Scholar
3.Rigosi, A., Carey, C. C., Ibelings, B. W. & Brookes, J. D. The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnol. Oceanogr. 59, 99–114 (2014).ADS
Google Scholar
4.Dokulil, M. T. & Teubner, K. Eutrophication and climate change: Present situation and future scenarios. In Eutrophication: Causes, Consequences and Control (eds Ansari, A. A. et al.) 1–16 (Springer, 2011).
Google Scholar
5.Codd, G. A., Lindsay, J., Young, F. M., Morrison, L. F. & Metcalf, J. S. Harmful Cyanobacteria (Springer, 2005).
Google Scholar
6.Harland, F. M. J., Wood, S. A., Moltchanova, E., Williamson, W. M. & Gaw, S. Phormidium autumnale growth and anatoxin-a production under iron and copper stress. Toxins (Basel). 5, 2504–2521 (2013).CAS
PubMed
PubMed Central
Google Scholar
7.Zurawell, R. W., Chen, H., Burke, J. M. & Prepas, E. E. Hepatotoxic cyanobacteria: A review of the biological importance of microcystins in freshwater environments. J. Toxicol. Environ. Health B 8, 1–37 (2005).CAS
Google Scholar
8.Funari, E. & Testai, E. Human health risk assessment related to cyanotoxins exposure. Crit. Rev. Toxicol. 38, 97–125 (2008).CAS
PubMed
Google Scholar
9.Brooks, B. W. et al. Are harmful algal blooms becoming the greatest inland water quality threat to public health and aquatic ecosystems?. Environ. Toxicol. Chem. 35, 6–13 (2016).CAS
PubMed
Google Scholar
10.Pick, F. R. & Lean, D. R. S. The role of macronutrients (C, N, P) in controlling cyanobacterial dominance in temperate lakes. N. Z. J. Mar. Freshw. Res. 21, 425–434 (1987).CAS
Google Scholar
11.Schindler, A. D. W. Evolution of phosphorus limitation in lakes. Science 195, 260–262 (1977).CAS
PubMed
ADS
Google Scholar
12.Kumar, K., Mella-Herrera, R. A. & Golden, J. W. Cyanobacterial heterocysts. Cold Spring Harb. Perspect. Biol. 2, 1–20 (2010).
Google Scholar
13.Paerl, H. W., Fulton, R. S., Moisander, P. H. & Dyble, J. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci. World J. 1, 76–113 (2001).CAS
Google Scholar
14.Paerl, H. W., Hall, N. S. & Calandrino, E. S. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci. Total Environ. 409, 1739–1745 (2011).CAS
PubMed
ADS
Google Scholar
15.Higgins, S. N. et al. Biological nitrogen fixation prevents the response of a eutrophic lake to reduced loading of nitrogen: Evidence from a 46-year whole-lake experiment. Ecosystems 21, 1088–1100 (2018).CAS
Google Scholar
16.Dolman, A. M. et al. Cyanobacteria and cyanotoxins: The influence of nitrogen versus phosphorus. PLoS ONE 7, e38757 (2012).CAS
PubMed
PubMed Central
ADS
Google Scholar
17.Schoffman, H., Lis, H., Shaked, Y. & Keren, N. Iron-nutrient interactions within phytoplankton. Front. Plant Sci. 7, 1223 (2016).PubMed
PubMed Central
Google Scholar
18.Needoba, J. A., Foster, R. A., Sakamoto, C., Zehr, J. P. & Johnson, K. S. Nitrogen fixation by unicellular diazotrophic cyanobacteria in the temperate oligotrophic North Pacific Ocean. Limnol. Oceanogr. 52, 1317–1327 (2007).CAS
ADS
Google Scholar
19.Romero, I. C., Klein, N. J., Sañudo-Wilhelmy, S. A. & Capone, D. G. Potential trace metal co-limitation controls on N2 fixation and NO3- uptake in lakes with varying trophic status. Front. Microbiol. 4, 1–12 (2013).CAS
Google Scholar
20.Newton, W. E. Physiology, biochemistry, and molecular biology of nitrogen fixation. In Biology of the Nitrogen Cycle 109–129 (Elsevier B. V, 2007).
Google Scholar
21.Salama, Z. A., El-Fouly, M. M., Lazova, G. & Popova, L. P. Carboxylating enzymes and carbonic anhydrase functions were suppressed by zinc deficiency in maize and chickpea plants. Acta Physiol. Plant. 28, 445–451 (2006).CAS
Google Scholar
22.Sültemeyer, D. Carbonic anhydrase in eukaryotic algae: Characterization, regulation, and possible function during photosynthesis. Can. J. Bot. 76, 962–972 (1998).
Google Scholar
23.Vallee, B. L. & Auld, D. S. Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29, 5647–5659 (1990).CAS
PubMed
Google Scholar
24.Wu, F. Y. & Wu, C. W. Zinc in DNA replication and transcription. Annu. Rev. Nutr. 7, 251–272 (1987).CAS
PubMed
Google Scholar
25.Beyer, W., Imlay, J. & Fridovich, I. Superoxide dismutases. Prog. Nucleic Acid Res. Mol. Biol. 40, 221–253 (1991).CAS
PubMed
Google Scholar
26.Holm-Hansen, O., Gerloff, G. H. & Skogg, F. Cobalt as an essential element for blue-green algae. Physiol. Plant. 7, 665–675 (1954).CAS
Google Scholar
27.Sunda, W. G. & Huntsman, S. A. Cobalt and zinc interreplacement in marine phytoplankton: Biological and geochemical implications. Limnol. Oceanogr. 40, 1404–1417 (1995).CAS
ADS
Google Scholar
28.Steffens, G. C. M., Biewald, R. & Buse, G. Cytochrome c oxidase is three-copper, two-heme-A protein. Eur. J. Biochem. 164, 295–300 (1987).CAS
PubMed
Google Scholar
29.Price, R. C., Mortimer, N., Smith, I. E. M. & Maas, R. Whole-rock geochemical reference data for Torlesse and Waipapa terranes, North Island, New Zealand. N. Z. J. Geol. Geophys. 58, 213–228 (2015).CAS
Google Scholar
30.Downs, T. M., Schallenberg, M. & Burns, C. W. Responses of lake phytoplankton to micronutrient enrichment: A study in two New Zealand lakes and an analysis of published data. Aquat. Sci. 70, 347–360 (2008).CAS
Google Scholar
31.Bayer, T. K., Schallenberg, M. & Martin, C. E. Investigation of nutrient limitation status and nutrient pathways in Lake Hayes, Otago, New Zealand: A case study for integrated lake assessment. N. Z. J. Mar. Freshw. Res. 42, 285–295 (2008).CAS
Google Scholar
32.Glass, J. B., Axler, R. P., Chandra, S. & Goldman, C. R. Molybdenum limitation of microbial nitrogen assimilation in aquatic ecosystems and pure cultures. Front. Microbiol. 3, 1–11 (2012).
Google Scholar
33.Sterner, R. W. et al. Phosphorus and trace metal limitation of algae and bacteria in Lake Superior. Limnol. Oceanogr. 49, 495–507 (2004).CAS
ADS
Google Scholar
34.Vrede, T. & Tranvik, L. J. Iron constraints on planktonic primary production in oligotrophic lakes. Ecosystems 9, 1094–1105 (2006).CAS
Google Scholar
35.North, R. L., Guildford, S. J., Smith, R. E. H., Havens, S. M. & Twiss, M. R. Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol. Oceanogr. 52, 315–328 (2007).CAS
ADS
Google Scholar
36.Kelly, L. T. et al. Trace metal and nitrogen concentrations differentially affect bloom forming cyanobacteria of the genus Dolichospermum. Aquat. Sci. 83, 1–11 (2021).
Google Scholar
37.Sorichetti, R. J., Creed, I. F. & Trick, C. G. Iron and iron-binding ligands as cofactors that limit cyanobacterial biomass across a lake trophic gradient. Freshw. Biol. 61, 146–157 (2016).CAS
Google Scholar
38.Wood, S. A. et al. Contrasting cyanobacterial communities and microcystin concentrations in summers with extreme weather events: Insights into potential effects of climate change. Hydrobiologia 785, 71–89 (2017).CAS
Google Scholar
39.Li, X., Dreher, T. W. & Li, R. An overview of diversity, occurrence, genetics and toxin production of bloom-forming Dolichospermum (Anabaena) species. Harmful Algae 54, 54–68 (2016).CAS
PubMed
Google Scholar
40.Hawes, I. & Smith, R. Seasonal dynamics of epilithic periphyton in oligotrophic lake Taupo, New Zealand. N. Z. J. Mar. Freshw. Res. 28, 1–12 (1994).
Google Scholar
41.Verburg, P. & Albert, A. Taupo Long Term Monitoring (Springer, 2018).
Google Scholar
42.Marañón, E. Cell Size as a key determinant of phytoplankton metabolism and community structure. Ann. Rev. Mar. Sci. 7, 241–264 (2015).PubMed
Google Scholar
43.Kagami, M. & Urabe, J. Phytoplankton growth rate as a function of cell size: An experimental test in Lake Biwa. Limnology 2, 111–117 (2001).
Google Scholar
44.Kraemer, S. M., Duckworth, O. W., Harrington, J. M. & Schenkeveld, W. D. C. Metallophores and trace metal biogeochemistry. Aquat. Geochem. 21, 159–195 (2015).CAS
Google Scholar
45.Twiss, M. R., Auclair, J.-C. & Charlton, M. N. An investigation into iron-stimulated phytoplankton productivity in epipelagic Lake Erie during thermal stratification using trace metal clean techniques. Can. J. Fish. Aquat. Sci. 57, 86–95 (2000).CAS
Google Scholar
46.Feng, Y., Fu, F. & Hutchins, D. A. Trace metal clean culture techniques. Res. Methods Environ. Physiol. Aquat. Sci. https://doi.org/10.1007/978-981-15-5354-7_36 (2021).Article
Google Scholar
47.Rhodes, L. et al. The Cawthron institute culture collection of micro-algae: A significant national collection. N. Z. J. Mar. Freshw. Res. 50, 291–316 (2016).
Google Scholar
48.Bolch, C. J. S. & Blackburn, S. I. Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kütz. J. Appl. Phycol. 8, 5–13 (1996).
Google Scholar
49.Worms, I., Simon, D. F., Hassler, C. S. & Wilkinson, K. J. Bioavailability of trace metals to aquatic microorganisms: Importance of chemical, biological and physical processes on biouptake. Biochimie 88, 1721–1731 (2006).CAS
PubMed
Google Scholar
50.Gobler, C. J., Hutchins, D. A., Fisher, N. S., Cosper, E. M. & Sañudo-Wilhelmy, S. A. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte. Limnol. Oceanogr. 42, 1492–1504 (1997).CAS
ADS
Google Scholar
51.Bell, W. & Mitchell, R. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol. Bull. 143, 265–277 (1972).
Google Scholar
52.Seymour, J. R., Amin, S. A., Raina, J. B. & Stocker, R. Zooming in on the phycosphere: The ecological interface for phytoplankton-bacteria relationships. Nat. Microbiol. 2, 65 (2017).
Google Scholar
53.Helliwell, K. E. et al. Cyanobacteria and eukaryotic algae use different chemical variants of Vitamin B12. Curr. Biol. 26, 999–1008 (2016).CAS
PubMed
PubMed Central
Google Scholar
54.Anderson, M. A. & Morel, F. M. M. The influence of aqueous iron chemistry on the uptake of iron by the coastal diatom Thallasiosira weissflogii. Limnol. Oceanogr. 27, 789–813 (1982).CAS
ADS
Google Scholar
55.Lis, H., Kranzler, C., Keren, N. & Shaked, Y. A comparative study of Iron uptake rates and mechanisms amongst marine and fresh water Cyanobacteria: Prevalence of reductive Iron uptake. Life 5, 841–860 (2015).CAS
PubMed
PubMed Central
Google Scholar
56.Bruland, K. W., Knauer, G. A. & Martin, J. H. Zinc in north-east Pacific water. Nature 271, 741–743 (1978).CAS
ADS
Google Scholar
57.Saeed, H. et al. Regulation of phosphorus bioavailability by iron nanoparticles in a monomictic lake. Sci. Rep. 8, 1–14 (2018).
Google Scholar
58.Baken, S., Degryse, F., Verheyen, L., Merckx, R. & Smolders, E. Metal complexation properties of freshwater dissolved organic matter are explained by its aromaticity and by anthropogenic ligands. Environ. Sci. Technol. 45, 2584–2590 (2011).CAS
PubMed
ADS
Google Scholar
59.Campbell, P. G. C. Interactions between trace metals and aquatic organisms: A critique of the free-ion activity model. In Metal Speciation and Bioavailability in Aquatic Systems (eds Tessier, A. & Turner, D. R.) 45–102 (Wiley, 1995).
Google Scholar
60.Scharek, R., Van Leeuwe, M. A. & De Baar, H. J. W. Responses of Southern Ocean phytoplankton to the addition of trace metals. Deep. Res. Part II 44, 209–227 (1997).CAS
Google Scholar
61.Facey, J. A., Apte, S. C. & Mitrovic, S. M. A review of the effect of trace metals on freshwater cyanobacterial growth and toxin production. Toxins (Basel). 11, 1–18 (2019).
Google Scholar
62.Zhang, X. et al. Effect of micronutrients on algae in different regions of Taihu, a large, spatially diverse, hypereutrophic lake. Water Res. 151, 500–514 (2019).CAS
PubMed
Google Scholar
63.Wever, A. D. et al. Differential response of phytoplankton to additions of nitrogen, phosphorus and iron in Lake Tanganyika. Freshw. Biol. 53, 264–277 (2008).
Google Scholar
64.Nalewajko, C. & Murphy, T. P. Effects of temperature, and availability of nitrogen and phosphorus on the abundance of Anabaena and Microcystis in Lake Biwa, Japan: An experimental approach. Limnology 2, 45–48 (2001).
Google Scholar
65.Kagami, M., Gurung, T. B., Yoshida, T. & Urabe, J. To sink or to be lysed? Contrasting fate of two large phytoplankton species in Lake Biwa. Limnol. Oceanogr. 51, 2775–2786 (2006).ADS
Google Scholar
66.Hartig, J. H. & Wallen, D. G. The influence of light and temperature on growth and photosynthesis of fragilaria crotonensis kitton. J. Freshw. Ecol. 3, 371–382 (1986).
Google Scholar
67.Tilman, D. Tests of resource competition theory using four species of Lake Michigan algae. Ecology 62, 802–815 (1981).
Google Scholar
68.Tompkins, T. & Blinn, D. W. The effect of mercury on the growth rate of Fragilaria crotonensis kitton and Asterionella formosa Hass. Hydrobiologia 49, 111–116 (1976).CAS
Google Scholar
69.Kazamia, E. et al. Endocytosis-mediated siderophore uptake as a strategy for Fe acquisition in diatoms. Sci. Adv. 4, aar4536 (2018).ADS
Google Scholar
70.Strzepek, R. F. & Harrison, P. J. Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431, 689–692 (2004).CAS
PubMed
ADS
Google Scholar
71.Strzepek, R. F., Boyd, P. W. & Sunda, W. G. Photosynthetic adaptation to low iron, light, and temperature in Southern Ocean phytoplankton. Proc. Natl. Acad. Sci. U. S. A. 116, 4388–4393 (2019).CAS
PubMed
PubMed Central
ADS
Google Scholar
72.Raven, J. A. The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol. 109, 279–287 (1988).CAS
Google Scholar
73.Kranzler, C., Rudolf, M., Keren, N. & Schleiff, E. Iron in cyanobacteria. Adv. Bot. Res. 65, 57–105 (2013).CAS
Google Scholar More