Diatom distribution and long-term survival in a heavily polluted sediment core from the Bay of Bagnoli (Tyrrhenian Sea, Italy)
Publiée :
Jan 8, 2025
Résumé
Diatom resting stages can remain viable in sediments for decades and germinate when exposed to suitable environmental conditions, inoculating the water column and the surface sediments with new populations of cells. Classical methods, based on acid-cleaning of diatom frustules in sediment samples, do not discriminate between living and dead cells and may destroy the more fragile taxa. We used a metabarcoding dataset based on the V9 region of the 18S rRNA (20,602 reads, 102 diatom Amplicon Sequence Variants (ASV)) coupled with the Serial Dilution Culture method to assess diversity and viability of resting stages in a heavily polluted sediment core from the Bay of Bagnoli (Tyrrhenian Sea) spanning approximately two centuries. Our results indicate that planktonic centric diatoms dominated the sediment layers, but ASVs of benthic pennates were also present, especially in older layers. High densities (up to ~2·106 cells g-1 wet sediment) of viable cells were recorded in the surface layer (dated to 2013) for Nanofrustulum shiloi and for a small unidentified pennate diatom. Concentrations of living cells decreased towards older layers, but cultures of Chaetoceros curvisetus were still generated from a layer dated to 1954. Selected strains were characterized morphologically, in light and electron microscopy, and molecularly, confirming the records of N. shiloi, Psammogramma sp. and Plagiogramma sp. The results of our study highlight the capability of several centric and pennate diatom species to ‘rest’ alive in severely polluted sediments for decades. This calls for future studies aimed at understanding the mechanisms that regulate dormancy and the adaptation to harsh environmental conditions, which have potential biotechnological applications.
Article Details
- Comment citer
-
PELUSI, A., ROMERO MARTÍNEZ, M. L., MULE, A., SCALCO, E., BARRENECHEA ANGELES, I., PIREDDA, R., KOOISTRA H.C.F. , W., MONTRESOR, M., & SARNO, D. (2025). Diatom distribution and long-term survival in a heavily polluted sediment core from the Bay of Bagnoli (Tyrrhenian Sea, Italy). Mediterranean Marine Science, 26(1), 40–54. https://doi.org/10.12681/mms.37946
- Rubrique
- Research Article
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Téléchargements
Les données relatives au téléchargement ne sont pas encore disponibles.
Références
Alverson, A.J., Jansen, R.K., Theriot, E.C., 2007. Bridging the Rubicon: Phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Molecular Phylogenetics and Evolution, 45, 193-210.
Amaral-Zettler, L.A., McCliment, E.A., Ducklow, H.W., Huse, S.M., 2009. A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS ONE, 4, e6372.
Andersen, P., Throndsen, J., 2003. Estimating cell numbers. p. 99-129 In: Manual on Harmful Marine Microalgae. Hallegraeff, G.M., Anderson, D.M., Cembella, A.D. (Eds). IOC-UNESCO, Paris.
Andersson, B., Godhe, A., Filipsson, H.L., Zetterholm, L., Edler, L. et al., 2022. Intraspecific variation in metal tolerance modulate competition between two marine diatoms. The Isme Journal, 16 (2), 511-520.
Andersson, B., Rengefors, K., Kourtchenko, O., Johannesson, K., Berglund, O. et al., 2023. Cross-contamination risks in sediment-based resurrection studies of phytoplankton. Limnology and Oceanography Letters, 8 (2), 376-384.
Anslan, S., Kang, W., Dulias, K., Wünnemann, B., Echeverría- Galindo, P. et al., 2022. Compatibility of diatom valve records with sedimentary ancient DNA amplicon data: A case study in a brackish, alkaline Tibetan lake. Frontiers in Earth Science, 10, 824656.
Armbrecht, L., Weber, M. E., Raymo, M.E., Peck, V.L., Williams, T. et al., 2022. Ancient marine sediment DNA reveals diatom transition in Antarctica. Nature Communications, 13 (1), 5787.
Armiento, G., Caprioli, R., Cerbone, A., Chiavarini, S., Crovato, C. et al., 2020. Current status of coastal sediments contamination in the former industrial area of Bagnoli-Coroglio (Naples, Italy). Chemistry and Ecology, 36 (6), 579-597.
Armiento, G., Barsanti, M., Caprioli, R., Chiavarini, S., Conte, F. et al., 2022. Heavy metal background levels and pollution temporal trend assessment within the marine sediments facing a brownfield area (Gulf of Pozzuoli, Southern Italy). Environmental Monitoring and Assessment, 194 (11), 814.
Barrenechea Angeles, I., Romero-Martínez, M. L., Cavaliere, M., Varrella, S., Francescangeli, F. et al., 2023. Encapsulated in sediments: eDNA deciphers the ecosystem history of one of the most polluted European marine sites. Environment International, 172, 107738.
Blaginina, A., Zheleznova, S., Miroshnichenko, E., Gevorgiz, R., Ryabushko, L., 2024. The Diatom Nanofrustulum shiloi As a Promising Species in Modern Biotechnology. Applied Biochemistry and Microbiology, 60 (3), 483-495.
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J. et al., 2009. BLAST+: architecture and applications. BMC Bioinformatics, 10 (1), 1-9.
Capo, E., Rydberg, J., Tolu, J., Domaizon, I., Debroas, D. et al., 2019. How Does Environmental Inter-annual Variability Shape Aquatic Microbial Communities? A 40-Year Annual Record of Sedimentary DNA From a Boreal Lake (Nylandssjon, Sweden). Frontiers in Ecology and Evolution, 7, 245.
Cullen, J.J., MacIntyre, H. L., 2016. On the use of the serial dilution culture method to enumerate viable phytoplankton in natural communities of plankton subjected to ballast water treatment. Journal of Applied Phycology (28), 279-298.
Dzhembekova, N., Moncheva, S., Ivanova, P., Slabakova, N., Nagai, S., 2018. Biodiversity of phytoplankton cyst assemblages in surface sediments of the Black Sea based on metabarcoding. Biotechnology & Biotechnological Equipment, 32 (6), 1507-1513.
Ellegaard, M., Ribeiro, S., 2018. The long-term persistence of phytoplankton resting stages in aquatic ‘seed banks’. Biological Reviews, 93 (1), 166-183.
Ellegaard, M., Clokie, M.R.J, Czypionka, T., Frisch, D., Godhe, A. et al., 2020. Dead or alive: sediment DNA archives as tools for tracking aquatic evolution and adaptation. Communications Biology, 3 (1), 169.
Gaonkar, C.C., Piredda, R., Minucci, C., Mann, D.G., Montresor, M. et al., 2018. Annotated 18S and 28S rDNA reference sequences of taxa in the planktonic diatom family Chaetocerotaceae. PLoS ONE, 13 (12), e0208929.
Guillou, L., Bachar, D., Audic, S., Bass, D., Berney, C. et al., 2012. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Research, 41 (D1), D597-D604.
Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series, 41, 95-98.
Haraguchi, L., Moestrup, Ø., Jakobsen, H.H., Lundholm, N., 2022. Phytoflagellate diversity in Roskilde Fjord (Denmark), including the description of Pyramimonas octopora sp. nov. (Pyramimonadales, Chlorophyta). Phycologia, 61 (1) 45-59.
Härnström, K., Ellegaard, M., Andersen, T.J., Godhe, A., 2011. Hundred years of genetic structure in a sediment revived diatom population. Proceedings of the National Academy of Sciences of the United States of America, 108 (10), 4252-4257.
Hattich, G.S.I., Jokinen, S., Sildever, S., Gareis, M., Heikkinen, J. et al., 2024. Temperature optima of a natural diatom population increases as global warming proceeds. Nature Climate Change, 14, 518-525.
Imai, I., Itoh, K., Anraku, M., 1984. Extinction dilution method for enumeration of dormant cells of red tide organisms in marine sediments. Bulletin of Plankton Society of Japan, 31, 123-124.
Ishii, K.-I., Iwataki, M., Matsuoka, K., Imai, I., 2011. Proposal of identification criteria for resting spores of Chaetoceros species (Bacillariophyceae) from a temperate coastal sea. Phycologia, 50 (4), 351-362.
Itakura, S., Imai, I., Itoh, K., 1997. ‘Seed bank’ of coastal planktonic diatoms in bottom sediments of Hiroshima Bay, Seto Inland Sea, Japan. Marine Biology, 128, 497-508.
Keck, F., Millet, L., Debroas, D., Etienne, D., Galop, D. et al., 2020. Assessing the response of micro-eukaryotic diversity to the Great Acceleration using lake sedimentary DNA. Nature Communications, 11 (1), 3831.
Kooistra, W.H.C.F., Sarno, D., Hernández-Becerril, D.U., Assmy, P., Di Prisco, C. et al., 2010. Comparative molecular and morphological phylogenetic analyses of taxa in the Chaetocerotaceae (Bacillariophyta). Phycologia, 5, 471-500.
Kremp, A., Hinners, J., Klais, R., Leppanen, A.P., Kallio, A., 2018. Patterns of vertical cyst distribution and survival in 100-year-old sediment archives of three spring dinoflagellate species from the Northern Baltic Sea. European Journal of Phycology, 53 (2), 135-145.
Lee, J.J., 2011. Diatoms as endosymbionts. p. 437-464 In: The Diatom World. Cellular Origin, Life in Extreme Habitats and Astrobiology.
Seckbach, J., Kociolek, P. (Eds). Springer, Dordrecht. Legrand, B., Miras, Y., Beauger, A., Dussauze, M., Latour, D., 2019. Akinetes and ancient DNA reveal toxic cyanobacterial recurrences and their potential for resurrection in a 6700-year-old core from a eutrophic lake. Science of the Total Environment, 687, 1369-1380.
Li, C.L., Witkowski, A., Ashworth, M.P., Dąbek, P., Sato, S. et al., 2018. The morphology and molecular phylogenetics of some marine diatom taxa within the Fragilariaceae, including twenty undescribed species and their relationship to Nanofrustulum, Opephora and Pseudostaurosira. Phytotaxa, 355 (1), 1-104.
Li, C., Ashworth, M.P., Mackiewicz, P., Dąbek, P., Witkowski, J. et al., 2020. Morphology, phylogeny, and molecular dating in Plagiogrammaceae family focused on Plagiogramma- Dimeregramma complex (Urneidophycidae, Bacillariophyceae). Molecular Phylogenetics and Evolution, 148, 106808.
Liu, L., Wang, Z., Lu, S., 2020. Diversity and geographical distribution of resting stages of eukaryotic algae in the surface sediments from the southern Chinese coastline based on metabarcoding partial 18S rDNA sequences. Marine Ecology, 41 (3), e12585.
Liu, C., Cui, Y., Li, X., Yao, M., 2021. microeco: an R package for data mining in microbial community ecology. FEMS Microbiology Ecology, 97 (2), fiaa255.
Lundholm, N., Ribeiro, S., Andersen, T.J., Koch, T., Godhe, A. et al., 2011. Buried alive - germination of up to a century-old marine protist resting stages. Phycologia, 50 (6), 629-640.
Marella, T.K., López-Pacheco, I.Y., Parra-Saldívar, R., Dixit, S., Tiwari, A., 2020. Wealth from waste: Diatoms as tools for phycoremediation of wastewater and for obtaining value from the biomass. Science of the Total Environment, 724, 137960.
Margiotta, F., Balestra, C., Buondonno, A., Casotti, R., D’Ambra, I. et al., 2020. Do plankton reflect the environmental quality status? The case of a postindustrial Mediterranean bay. Marine Enviromental Research, 160, 104980.
Martínez, Y.J., Siqueiros-Beltrones, D.A., Marmolejo- Rodríguez, A.J., 2021. Response of Benthic Diatom Assemblages to Contamination by Metals in a Marine Environment. Journal of Marine Science and Engineering, 9 (4), 443.
McMurdie, P.J., Holmes, S., 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8 (4), e61217.
McQuoid, M.R., 2002. Pelagic and benthic environmental controls on the spatial distribution of a viable diatom propagule bank on the Swedish west coast. Journal of Phycology, 38, 881-893.
McQuoid, M.R., Godhe, A., Nordberg, K., 2002. Viability of phytoplankton resting stages in the sediments of a coastal Swedish fjord. European Journal of Phycology, 37, 191-201.
McQuoid, M.R., Hobson, L.A., 1996. Diatom resting stages. Journal of Phycology, 32 (6).
Mišić Radić, T., Čačković, A., Penezić, A., Dautović, J., Lončar, J. et al., 2021. Physiological and morphological response of marine diatom Cylindrotheca closterium (Bacillariophyceae) exposed to cadmium. European Journal of Phycology, 56 (1), 24-36.
Montresor, M., Di Prisco, C., Sarno, D., Margiotta, F., Zingone, A., 2013. Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Marine Ecology Progress Series, 484, 79-95.
Mucko, M., Bosak, S., Mann, D.G., Trobajo, R., Wetzel, C. E. et al., 2021. A polyphasic approach to the study of the genus Nitzschia (Bacillariophyta): three new planktonic species from the Adriatic Sea. Journal of Phycology, 57 (1), 143-159.
Nanjappa, D., Kooistra, W.H.C.F., Zingone, A., 2013. A reappraisal of the genus Leptocylindrus (Bacillariophyta), with the addition of three species and the erection of Tenuicylindrus gen. nov. Journal of Phycology, 49, 917-936.
Othman, H.B., Pick, F.R., Hlaili, A.S., Leboulanger, C., 2023. Effects of polycyclic aromatic hydrocarbons on marine and freshwater microalgae–A review. Journal of Hazardous Materials, 441, 129869.
Pawlowski, J., Bruce, K., Panksep, K., Aguirre, F.I., Amalfitano, S. et al., 2022. Environmental DNA metabarcoding for benthic monitoring: A review of sediment sampling and DNA extraction methods. Science of the Total Environment, 818, 151783.
Pérez-Burillo, J., Valoti, G., Witkowski, A., Prado, P., Mann, D.G. et al., 2022. Assessment of marine benthic diatom communities: insights from a combined morphological– metabarcoding approach in Mediterranean shallow coastal waters. Marine Pollution Bulletin, 174, 113183.
Piredda, R., Sarno, D., Lange, C. B., Tomasino, M. P., Zingone, A. et al., 2017. Diatom resting stages in surface sediments: a pilot study comparing Next Generation Sequencing and Serial Dilution Cultures. Cryptogamie Algologie, 38, 31-46.
Piredda, R., Claverie, J.-M., Decelle, J., de Vargas, C., Dunthorn, M. et al., 2018. Diatom diversity through HTS-metabarcoding in coastal European seas. Scientific Reports, 8 (1), 18059.
Prazeres, M., Renema, W., 2019. Evolutionary significance of the microbial assemblages of large benthic Foraminifera. Biological Reviews, 94 (3), 828-848.
Rimet, F., Gusev, E., Kahlert, M., Kelly, M.G., Kulikovskiy, M. et al., 2019. Diat.barcode, an open-access curated barcode library for diatoms. Scientific Reports, 9 (1), 15116.
Sar, E.A., Sunesen, I., 2003. Nanofrustulum shiloi (Bacillariophyceae) from the Gulf of San Matìas (Agrgentina): Morphology, distribution and comments about nomenclature. Nova Hedwigia, 77 (3-4), 399-406.
Sarno, D., Kooistra, W.H.C.F., Medlin, L. K., Percopo, I., Zingone, A., 2005. Diversity in the genus Skeletonema (Bacillariophyceae). II. An assessment of the taxonomy of S. costatum-like species, with the description of four new species. Journal of Phycology, 41, 151-176.
Sarno, D., Kooistra, W.H.C.F., Balzano, S., Hargraves, P. E., Zingone, A., 2007. Diversity in the genus Skeletonema (Bacillariophyceae): III. Phylogenetic position and morphological variability of Skeletonema costatum and Skeletonema grevillei, with the description of Skeletonema ardens sp. nov. Journal of Phycology, 43, 156-170.
Sato, S., Kooistra, W.H.C.F., Watanabe, T., Matsumoto, S., Medlin, L.K., 2008. A new araphid diatom genus Psammoneis gen. nov. (Plagiogrammaceae, Bacillariophyta) with three new species based on SSU and LSU rDNA sequence data and morphology. Phycologia, 47 (5), 510-528.
Siano, R., Lassudrie, M., Cuzin, P., Briant, N., Loizeau, V. et al., 2021. Sediment archives reveal irreversible shifts in plankton communities after World War II and agricultural pollution. Current Biology, 31, 2682–2689.
Sims, P.A., Ashworth, M.P., Theriot, E.C., Manning, S.R., 2023. Molecular and morphological analysis of Biddulphia sensu lato: a new diagnosis of Biddulphia, with a description of the new genera Biddulphiella and Neobrightwellia. Marine Micropaleontology, 178, 102186.
Singh, P., Teixeira, J.C., Bolch, C., Armbrecht, L., 2024. Marine sedimentary ancient DNA from Antarctic diatoms. Palaeogeography, Palaeoclimatology, Palaeoecology, 640, 112090.
Sprovieri, M., Passaro, S., Ausili, A., Bergamin, L., Finoia, M.G. et al., 2020. Integrated approach of multiple environmental datasets for the assessment of sediment contamination in marine areas affected by long-lasting industrial activity: the case study of Bagnoli (southern Italy). Journal of Soils and Sediments, 20 (3), 1692-1705.
Turk Dermastia, T., Vascotto, I., Francé, J., Stanković, D., Mozetič, P., 2023. Evaluation of the rbcL marker for metabarcoding of marine diatoms and inference of population structure of selected genera. Frontiers in Microbiology, 14, 1071379.
van der Loos, L.M., Nijland, R., 2021. Biases in bulk: DNA metabarcoding of marine communities and the methodology involved. Molecular Ecology, 30 (13), 3270-3288.
Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer International Publishing Cham, 12 pp.
Witkowski, A., Li, C., Zgłobicka, I., Yu, S.-X., Ashworth, M. et al., 2016. Multigene assessment of biodiversity of diatom (Bacillariophyceae) assemblages from the littoral zone of the Bohai and Yellow Seas in Yantai Region of Northeast China with some remarks on ubiquitous taxa. Journal of Coastal Research (74), 166-195.
Wood, S.M., Kremp, A., Savela, H., Akter, S., Vartti, V.P. et al., 2021. Cyanobacterial Akinete Distribution, Viability, and Cyanotoxin Records in Sediment Archives From the Northern Baltic Sea. Frontiers in Microbiology, 12, 681881.
Zimmermann, H.H., Stoof‐Leichsenring, K.R., Kruse, S., Nürnberg, D., Tiedemann, R. et al., 2021. Sedimentary ancient DNA from the Subarctic North Pacific: how sea ice, salinity, and insolation dynamics have shaped diatom composition and richness over the past 20,000 Years. Paleoceanography and Paleoclimatology, 36 (4), e2020PA004091.
