Highly branched isoprenoids: a novel tracer of diatom-based energy pathways in freshwater food webs
Sydney Wilkinson
A C , Thomas Brown B and Bailey C. McMeans A
+ Author Affiliations
- Author Affiliations
A University of Toronto Mississauga, 3359 Mississauga Road, Mississauga, ON, L5L 1C6, Canada.
B Scottish Association for Marine Science, Oban, Argyll, PA37 1QA, UK.
C Corresponding author. Email: wilkinson.syd@gmail.com
Marine and Freshwater Research - https://doi.org/10.1071/MF20059
Submitted: 24 February 2020 Accepted: 1 July 2020 Published online: 12 August 2020
Abstract
In complex food webs, it is often difficult to classify all trophic interactions, especially when the number of potential energy sources and interacting species can be high. Biochemical markers (biomarkers) can help trace energy-flow pathways from basal sources up to top predators, but can suffer from poor resolution when multiple sources all produce the same biomarker (e.g. many algae produce long-chain unsaturated fatty acids). Highly branched isoprenoids (HBIs) are unique lipids produced by diatoms, which have been successfully applied as biomarkers of diatom-derived energy pathways through marine food webs. However, currently, the existence and trophic transfer of HBIs has not been explored in freshwater food webs. Here, we confirm, for the first time, the presence of two HBI isomers (IIb and IIc) across two temperate-lake food webs, from lower basal sources up to higher trophic-position consumers (predatory fishes). Lake ecosystems are facing multiple interacting threats that could influence food-web structure and function in complex ways. HBIs could provide a novel method for tracing the outcome of altered temperature, nutrient loading and water clarity on high-quality, diatom-derived energy pathways through freshwater food webs.
Keywords: algae, biomarker, consumer, diatom, freshwater, food web, highly branched isoprenoids, trophic-level.
References
Aichner, B., Wilkes, H., Herzschuh, U., Mischke, S., and Zhang, C. (2010). Biomarker and compound-specific δ13C evidence for changing environmental conditions and carbon limitation at Lake Koucha, eastern Tibetan Plateau. Journal of Paleolimnology 43, 873–899.| Biomarker and compound-specific δ13C evidence for changing environmental conditions and carbon limitation at Lake Koucha, eastern Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |
Athanasakoglou, A., and Kampranis, S. C. (2019). Diatom isoprenoids: advances and biotechnological potential. Biotechnology Advances 37, 107417.
| Diatom isoprenoids: advances and biotechnological potential.Crossref | GoogleScholarGoogle Scholar | 31326522PubMed |
Bates, D., Mächler, M., Bolker, B., and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Beardall, J., and Stojkovic, S. (2006). Microalgae under global environmental change: implications for growth and productivity, populations and trophic flow. ScienceAsia 32, 001–010.
| Microalgae under global environmental change: implications for growth and productivity, populations and trophic flow.Crossref | GoogleScholarGoogle Scholar |
Belt, S. T. (2018). Source-specific biomarkers as proxies for Arctic and Antarctic sea ice. Organic Geochemistry 125, 277–298.
| Source-specific biomarkers as proxies for Arctic and Antarctic sea ice.Crossref | GoogleScholarGoogle Scholar |
Belt, S. T., Cooke, D. A., Robert, J. M., and Rowland, S. (1996). Structural characterisation of widespread polyunsaturated isoprenoid biomarkers: a C25 triene, tetraene and pentaene from the diatom Haslea ostrearia simonsen. Tetrahedron Letters 37, 4755–4758.
| Structural characterisation of widespread polyunsaturated isoprenoid biomarkers: a C25 triene, tetraene and pentaene from the diatom Haslea ostrearia simonsen.Crossref | GoogleScholarGoogle Scholar |
Belt, S. T., Massé, G., Allard, W. G., Robert, J. M., and Rowland, S. J. (2001). Identification of a C25 highly branched isoprenoid triene in the freshwater diatom Navicula sclesvicensis. Organic Geochemistry 32, 1169–1172.
| Identification of a C25 highly branched isoprenoid triene in the freshwater diatom Navicula sclesvicensis.Crossref | GoogleScholarGoogle Scholar |
Belt, S. T., Brown, T. A., Rodriguez, A. N., Sanz, P. C., Tonkin, A., and Ingle, R. (2012). A reproducible method for the extraction, identification and quantification of the Arctic sea ice proxy IP25 from marine sediments. Analytical Methods 4, 705–713.
| A reproducible method for the extraction, identification and quantification of the Arctic sea ice proxy IP25 from marine sediments.Crossref | GoogleScholarGoogle Scholar |
Brett, M. T., Bunn, S. E., Chandra, S., Galloway, A. W. E., Guo, F., Kainz, M. J., Kankaala, P., Lau, D. C. P., Moulton, T. P., Power, M. E., Rasmussen, J. B., Taipale, S. J., Thorp, J. H., and Wehr, J. D. (2017). How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshwater Biology 62, 833–853.
| How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems?Crossref | GoogleScholarGoogle Scholar |
Brown, T. A. (2018). Stability of the lipid biomarker H-Print within preserved animals. Polar Biology 41, 1901–1905.
| Stability of the lipid biomarker H-Print within preserved animals.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., and Belt, S. T. (2012). Identification of the sea ice diatom biomarker IP25 in Arctic benthic macrofauna: direct evidence for a sea ice diatom diet in Arctic heterotrophs. Polar Biology 35, 131–137.
| Identification of the sea ice diatom biomarker IP25 in Arctic benthic macrofauna: direct evidence for a sea ice diatom diet in Arctic heterotrophs.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., and Belt, S. T. (2017). Biomarker-based H-Print quantifies the composition of mixed sympagic and pelagic algae consumed by Artemia sp. Journal of Experimental Marine Biology and Ecology 488, 32–37.
| Biomarker-based H-Print quantifies the composition of mixed sympagic and pelagic algae consumed by Artemia sp.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., Belt, S. T., and Piepenburg, D. (2012). Evidence for a pan-Arctic sea-ice diatom diet in Strongylocentrotus spp. Polar Biology 35, 1281–1287.
| Evidence for a pan-Arctic sea-ice diatom diet in Strongylocentrotus spp.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., Belt, S. T., Ferguson, S. H., Yurkowski, D. J., Davison, N. J., Barnett, J. E. F., and Jepson, P. D. (2013a). Identification of the sea ice diatom biomarker IP25 and related lipids in marine mammals: a potential method for investigating regional variations in dietary sources within higher trophic level marine systems. Journal of Experimental Marine Biology and Ecology 441, 99–104.
| Identification of the sea ice diatom biomarker IP25 and related lipids in marine mammals: a potential method for investigating regional variations in dietary sources within higher trophic level marine systems.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., Bicknell, A. W. J., Votier, S. C., and Belt, S. T. (2013b). Novel molecular fingerprinting of marine avian diet provides a tool for gaining insights into feeding ecology. Environmental Chemistry Letters 11, 283–288.
| Novel molecular fingerprinting of marine avian diet provides a tool for gaining insights into feeding ecology.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., Belt, S. T., Tatarek, A., and Mundy, C. J. (2014a). Source identification of the Arctic sea ice proxy IP25. Nature Communications 5, 4197–4202.
| Source identification of the Arctic sea ice proxy IP25.Crossref | GoogleScholarGoogle Scholar | 24939562PubMed |
Brown, T. A., Yurkowski, D. J., Ferguson, S. H., Alexander, C., and Belt, S. T. (2014b). H-Print: a new chemical fingerprinting approach for distinguishing primary production sources in Arctic ecosystems. Environmental Chemistry Letters 12, 455–460.
| H-Print: a new chemical fingerprinting approach for distinguishing primary production sources in Arctic ecosystems.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., Hegseth, E. N., and Belt, S. T. (2015). A biomarker-based investigation of the mid-winter ecosystem in Rijpfjorden, Svalbard. Polar Biology 38, 37–50.
| A biomarker-based investigation of the mid-winter ecosystem in Rijpfjorden, Svalbard.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., Chrystal, E., Ferguson, S. H., Yurkowski, D. J., Watt, C., Hussey, N. E., Kelley, T. C., and Belt, S. T. (2017). Coupled changes between the H-Print biomarker and δ15N indicates a variable sea ice carbon contribution to the diet of Cumberland Sound beluga whales. Limnology and Oceanography 62, 1606–1619.
| Coupled changes between the H-Print biomarker and δ15N indicates a variable sea ice carbon contribution to the diet of Cumberland Sound beluga whales.Crossref | GoogleScholarGoogle Scholar |
Brown, T. A., Galicia, M. P., Thiemann, G. W., Belt, S. T., Yurkowski, D. J., and Dyck, M. G. (2018). High contributions of sea ice derived carbon in polar bear (Ursus maritimus) tissue. PLoS One 13, e0191631.
| High contributions of sea ice derived carbon in polar bear (Ursus maritimus) tissue.Crossref | GoogleScholarGoogle Scholar | 29360849PubMed |
Colombo, S. M., Rodgers, T. F. M., Diamond, M. L., Bazinet, R. P., and Arts, M. T. (2019). Projected declines in global DHA availability for human consumption as a result of global warming. Ambio 37, 1–16.
Cyr, H. (2017). Winds and the distribution of nearshore phytoplankton in a stratified lake. Water Research 122, 114–127.
| Winds and the distribution of nearshore phytoplankton in a stratified lake.Crossref | GoogleScholarGoogle Scholar | 28595122PubMed |
Doucett, R. R., Marks, J. C., Blinn, D. W., Caron, M., and Hungate, B. A. (2007). Measuring terrestrial subsidies to aquatic food webs using stable isotopes of hydrogen. Ecology 88, 1587–1592.
| Measuring terrestrial subsidies to aquatic food webs using stable isotopes of hydrogen.Crossref | GoogleScholarGoogle Scholar | 17601150PubMed |
Elsner, M., Jochmann, M. A., Hofstetter, T. B., Hunkeler, D., Bernstein, A., Schmidt, T. C., and Schimmelmann, A. (2012). Current challenges in compound-specific stable isotope analysis of environmental organic contaminants. Analytical and Bioanalytical Chemistry 403, 2471–2491.
| Current challenges in compound-specific stable isotope analysis of environmental organic contaminants.Crossref | GoogleScholarGoogle Scholar | 22302163PubMed |
Finlay, J. C., Power, M. E., and Cabana, G. (1999). Effects of water velocity on algal carbon isotope ratios: Implications for river food web studies. Limnology and Oceanography 44, 1198–1203.
| Effects of water velocity on algal carbon isotope ratios: Implications for river food web studies.Crossref | GoogleScholarGoogle Scholar |
Goutte, A., Cherel, Y., Houssais, M. N., Klein, V., Ozouf-Costaz, C., Raccurt, M., Robineau, C., and Massé, G. (2013). Diatom-specific highly branched isoprenoids as biomarkers in Antarctic consumers. PLoS One 8, e56504.
| Diatom-specific highly branched isoprenoids as biomarkers in Antarctic consumers.Crossref | GoogleScholarGoogle Scholar | 23418580PubMed |
He, D., Simoneit, B. R. T., Xu, Y., and Jaffé, R. (2016). Occurrence of unsaturated C25 highly branched isoprenoids (HBIs) in a freshwater wetland. Organic Geochemistry 93, 59–67.
| Occurrence of unsaturated C25 highly branched isoprenoids (HBIs) in a freshwater wetland.Crossref | GoogleScholarGoogle Scholar |
Henderson, R. J., and Tocher, D. R. (1987). The lipid composition and biochemistry of freshwater fish. Progress in Lipid Research 26, 281–347.
| The lipid composition and biochemistry of freshwater fish.Crossref | GoogleScholarGoogle Scholar | 3324105PubMed |
Kainz, M., Arts, M. T., and Mazumder, A. (2004). Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnology and Oceanography 49, 1784–1793.
| Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels.Crossref | GoogleScholarGoogle Scholar |
McCann, K. S., and Rooney, N. (2009). The more food webs change, the more they stay the same. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 364, 1789–1801.
| The more food webs change, the more they stay the same.Crossref | GoogleScholarGoogle Scholar | 19451128PubMed |
Peng, C. Y. J., Lee, K. L., and Ingersoll, G. M. (2002). An introduction to logistic regression analysis and reporting. The Journal of Educational Research 96, 3–14.
| An introduction to logistic regression analysis and reporting.Crossref | GoogleScholarGoogle Scholar |
Rowland, S. J. (1983). Origins and fate of sedimentary isoprenoids. Ph.D. Thesis, University of Bristol, UK.
Rühland, K. M., Paterson, A. M., and Smol, J. P. (2015). Lake diatom responses to warming: reviewing the evidence. Journal of Paleolimnology 54, 1–35.
| Lake diatom responses to warming: reviewing the evidence.Crossref | GoogleScholarGoogle Scholar |
Schmidt, T. C., Zwank, L., Elsner, M., Berg, M., Meckenstock, R. U., and Haderlein, S. B. (2004). Compound-specific stable isotope analysis of organic contaminants in natural environments: a critical review of the state of the art, prospects, and future challenges. Analytical and Bioanalytical Chemistry 378, 283–300.
| Compound-specific stable isotope analysis of organic contaminants in natural environments: a critical review of the state of the art, prospects, and future challenges.Crossref | GoogleScholarGoogle Scholar | 14647941PubMed |
St Jacques, J. M., Douglas, M. S. V., Price, N., Drakulic, N., and Gubala, C. P. (2005). The effect of fish introductions on the diatom and cladoceran communities of Lake Opeongo, Ontario, Canada. Hydrobiologia 549, 99–113.
| The effect of fish introductions on the diatom and cladoceran communities of Lake Opeongo, Ontario, Canada.Crossref | GoogleScholarGoogle Scholar |
Taipale, S., Strandberg, U., Peltomaa, E., Galloway, A. W. E., Ojala, A., and Brett, M. T. (2013). Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes. Aquatic Microbial Ecology 71, 165–178.
| Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes.Crossref | GoogleScholarGoogle Scholar |
Taipale, S. J., Vuorio, K., Brett, M. T., Peltomaa, E., Hiltunen, M., and Kankaala, P. (2016a). Lake zooplankton δ13C values are strongly correlated with the δ13C values of distinct phytoplankton taxa. Ecosphere 7, e01392.
| Lake zooplankton δ13C values are strongly correlated with the δ13C values of distinct phytoplankton taxa.Crossref | GoogleScholarGoogle Scholar |
Taipale, S. J., Vuorio, K., Strandberg, U., Kahilainen, K. K., Järvinen, M., Hiltunen, M., Peltomaa, E., and Kankaala, P. (2016b). Lake eutrophication and brownification downgrade availability and transfer of essential fatty acids for human consumption. Environment International 96, 156–166.
| Lake eutrophication and brownification downgrade availability and transfer of essential fatty acids for human consumption.Crossref | GoogleScholarGoogle Scholar | 27685803PubMed |
Tocher, D. R. (2003). Metabolism and functions of lipids and fatty acids in teleost fish. Reviews in Fisheries Science 11, 107–184.
| Metabolism and functions of lipids and fatty acids in teleost fish.Crossref | GoogleScholarGoogle Scholar |
Vadeboncoeur, Y., Jeppesen, E., Vander Zanden, M. J., Schierup, H. H., Christoffersen, K., and Lodge, D. M. (2003). From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnology and Oceanography 48, 1408–1418.
| From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes.Crossref | GoogleScholarGoogle Scholar |
Volkman, J. K., Barrett, S. M., and Dunstan, G. A. (1994). C25 and C30 highly branched isoprenoid alkenes in laboratory cultures of two marine diatoms. Organic Geochemistry 21, 407–414.
| C25 and C30 highly branched isoprenoid alkenes in laboratory cultures of two marine diatoms.Crossref | GoogleScholarGoogle Scholar |
Zhang, Z., Metzger, P., and Sachs, J. P. (2011). Co-occurrence of long chain diols, keto-ols, hydroxy acids and keto acids in recent sediments of Lake El Junco, Galápagos Islands. Organic Geochemistry 42, 823–837.
| Co-occurrence of long chain diols, keto-ols, hydroxy acids and keto acids in recent sediments of Lake El Junco, Galápagos Islands.Crossref | GoogleScholarGoogle Scholar |
