Seasonal development of a tidal mixing front drives shifts in community structure and diversity of bacterioplankton.

16S sequencing Celtic Sea front Shallow Sea front microbial biogeography microbiome

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
09 2023
Historique:
revised: 25 07 2023
received: 19 04 2023
accepted: 28 07 2023
medline: 6 9 2023
pubmed: 9 8 2023
entrez: 9 8 2023
Statut: ppublish

Résumé

Bacterioplankton underpin biogeochemical cycles and an improved understanding of the patterns and drivers of variability in their distribution is needed to determine their wider functioning and importance. Sharp environmental gradients and dispersal barriers associated with ocean fronts are emerging as key determinants of bacterioplankton biodiversity patterns. We examined how the development of the Celtic Sea Front (CF), a tidal mixing front on the Northwest European Shelf affects bacterioplankton communities. We performed 16S-rRNA metabarcoding on 60 seawater samples collected from three depths (surface, 20 m and seafloor), across two research cruises (May and September 2018), encompassing the intra-annual range of the CF intensity. Communities above the thermocline of stratified frontal waters were clearly differentiated and less diverse than those below the thermocline and communities in the well-mixed waters of the Irish Sea. This effect was much more pronounced in September, when the CF was at its peak intensity. The stratified zone likely represents a stressful environment for bacterioplankton due to a combination of high temperatures and low nutrients, which fewer taxa can tolerate. Much of the observed variation was driven by Synechococcus spp. (cyanobacteria), which were more abundant within the stratified zone and are known to thrive in warm oligotrophic waters. Synechococcus spp. are key contributors to global primary productivity and carbon cycling and, as such, variability driven by the CF is likely to influence regional biogeochemical processes. However, further studies are required to explicitly link shifts in community structure to function and quantify their wider importance to pelagic ecosystems.

Identifiants

pubmed: 37555658
doi: 10.1111/mec.17097
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5201-5210

Informations de copyright

© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Références

Alderkamp, A., Sintes, E., & Herndl, G. J. (2006). Abundance and activity of major groups of prokaryotic plankton in the coastal North Sea during spring and summer. Aquatic Microbial Ecology, 45(3), 237-246.
Allen, R., Summerfield, T. C., Currie, K., Dillingham, P. W., & Hoffmann, L. J. (2020). Distinct processes structure bacterioplankton and protist communities across an oceanic front. Aquatic Microbial Ecology, 85, 19-34.
Arrigo, K. R. (2005). Marine microorganisms and global nutrient cycles. Nature, 437(7057), 349-355.
Baltar, F., Arístegui, J., Gasol, J. M., Lekunberri, I., & Herndl, G. J. (2010). Mesoscale eddies: Hotspots of prokaryotic activity and differential community structure in the ocean. The ISME Journal, 4(8), 975-988.
Baltar, F., Currie, K., Stuck, E., Roosa, S., & Morales, S. E. (2016). Oceanic fronts: Transition zones for bacterioplankton community composition. Environmental Microbiology Reports, 8(1), 132-138.
Belkin, I. M., Cornillon, P. C., & Sherman, K. (2009). Fronts in large marine ecosystems. Progress in Oceanography, 81(1-4), 223-236.
Birrien, J., Wafar, M., Corre, P. L., & Riso, R. (1991). Nutrients and primary production in a shallow stratified ecosystem in the Iroise Sea. Journal of Plankton Research, 13(4), 721-742.
Bolaños, L. M., Choi, C. J., Worden, A. Z., Baetge, N., Carlson, C. A., & Giovannoni, S. (2021). Seasonality of the microbial community composition in the North Atlantic. Frontiers in Marine Science, 8, 624164.
Bunse, C., & Pinhassi, J. (2017). Marine bacterioplankton seasonal succession dynamics. Trends in Microbiology, 25(6), 494-505.
Cadier, M., Gorgues, T., Sourisseau, M., Edwards, C. A., Aumont, O., Marié, L., & Memery, L. (2017). Assessing spatial and temporal variability of phytoplankton communities' composition in the Iroise Sea ecosystem (Brittany, France): A 3D modeling approach. Part 1: Biophysical control over plankton functional types succession and distribution. Journal of Marine Systems, 165, 47-68.
Callahan, B. J., Sankaran, K., Fukuyama, J. A., McMurdie, P. J., & Holmes, S. P. (2016). Bioconductor workflow for microbiome data analysis: From raw reads to community analyses. F1000Research, 5, 5.
Camarena-Gómez, M. T., Lipsewers, T., Piiparinen, J., Eronen-Rasimus, E., Perez-Quemaliños, D., Hoikkala, L., Sobrino, C., & Spilling, K. (2018). Shifts in phytoplankton community structure modify bacterial production, abundance and community composition. Aquatic Microbial Ecology, 81(2), 149-170.
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11, 265-270.
Chase, J. M. (2007). Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences, 104(44), 17430-17434.
Djurhuus, A., Boersch-Supan, P. H., Mikalsen, S.-O., & Rogers, A. D. (2017). Microbe biogeography tracks water masses in a dynamic oceanic frontal system. Royal Society Open Science, 4(3), 170033.
Fadeev, E., Wietz, M., von Appen, W. J., Iversen, M. H., Nöthig, E. M., Engel, A., Grosse, J., Graeve, M., & Boetius, A. (2021). Submesoscale physicochemical dynamics directly shape bacterioplankton community structure in space and time. Limnology and Oceanography, 66(7), 2901-2913.
Falkowski, P. G., Fenchel, T., & Delong, E. F. (2008). The microbial engines that drive Earth's biogeochemical cycles. Science, 320(5879), 1034-1039.
Flombaum, P., Gallegos, J. L., Gordillo, R. A., Rincón, J., Zabala, L. L., Jiao, N., Karl, D. M., Li, W. K., Lomas, M. W., Veneziano, D., & Vera, C. S. (2013). Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences, 110(24), 9824-9829.
Franks, P. J. (1992a). Phytoplankton blooms at fronts: Patterns, scales, and physical forcing mechanisms. Reviews in Aquatic Sciences, 6(2), 121-137.
Franks, P. J. (1992b). Sink or swim: Accumulation of biomass at fronts. Marine Ecology Progress Series. Oldendorf, 82(1), 1-12.
Fuhrman, J. A., Cram, J. A., & Needham, D. M. (2015). Marine microbial community dynamics and their ecological interpretation. Nature Reviews Microbiology, 13(3), 133-146.
Galand, P. E., Pereira, O., Hochart, C., Auguet, J. C., & Debroas, D. (2018). A strong link between marine microbial community composition and function challenges the idea of functional redundancy. The ISME Journal, 12(10), 2470-2478.
Grepma, G. (1988). A physical, chemical and biological characterization of the Ushant tidal front. Internationale Revue der Gesamten Hydrobiologie und Hydrographie, 73(5), 511-536.
Griffiths, S. M., Harrison, X. A., Weldon, C., Wood, M. D., Pretorius, A., Hopkins, K., Fox, G., Preziosi, R. F., & Antwis, R. E. (2018). Genetic variability and ontogeny predict microbiome structure in a disease-challenged montane amphibian. The ISME Journal, 12(10), 2506-2517.
Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C., & Martiny, J. B. (2012). Beyond biogeographic patterns: Processes shaping the microbial landscape. Nature Reviews Microbiology, 10(7), 497-506.
Hernando-Morales, V., Ameneiro, J., & Teira, E. (2017). Water mass mixing shapes bacterial biogeography in a highly hydrodynamic region of the S outhern O cean. Environmental Microbiology, 19(3), 1017-1029.
Hewson, I., Steele, J. A., Capone, D. G., & Fuhrman, J. A. (2006). Temporal and spatial scales of variation in bacterioplankton assemblages of oligotrophic surface waters. Marine Ecology Progress Series, 311, 67-77.
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013). Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environmental Microbiology, 79(17), 5112-5120.
Le Fevre, J. (1987). Aspects of the biology of frontal systems. In Advances in marine biology (Vol. 23, pp. 163-299). Elsevier.
Lemonnier, C., Perennou, M., Eveillard, D., Fernandez-Guerra, A., Leynaert, A., Marié, L., Paillard, C., & Maignien, L. (2020). Linking spatial and temporal dynamic of bacterioplankton communities with ecological strategies across a coastal frontal area. Frontiers in Marine Science, 7, 376.
Lévy, M., Franks, P. J., & Smith, K. S. (2018). The role of submesoscale currents in structuring marine ecosystems. Nature Communications, 9(1), 1-16.
Li, W. K. (1994). Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting. Limnology and Oceanography, 39(1), 169-175.
Martin, A. P., Zubkov, M. V., Burkill, P. H., & Holland, R. J. (2005). Extreme spatial variability in marine picoplankton and its consequences for interpreting Eulerian time-series. Biology Letters, 1(3), 366-369.
Martin, A. P., Zubkov, M. V., Fasham, M. J., Burkill, P. H., & Holland, R. J. (2008). Microbial spatial variability: An example from the Celtic Sea. Progress in Oceanography, 76(4), 443-465.
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.
Meng, S., Peng, T., Liu, X., Wang, H., Huang, T., Gu, J.-D., & Hu, Z. (2022). Ecological role of bacteria involved in the biogeochemical cycles of mangroves based on functional genes detected through GeoChip 5.0. Msphere, 7(1), e00936-e00921.
Menge, B. A., Olson, A. M., & Dahlhoff, E. P. (2002). Environmental stress, bottom-up effects, and community dynamics: Integrating molecular-physiological and ecological approaches. Integrative and Comparative Biology, 42(4), 892-908.
Morales, S. E., Biswas, A., Herndl, G. J., & Baltar, F. (2019). Global structuring of phylogenetic and functional diversity of pelagic fungi by depth and temperature. Frontiers in Marine Science, 6, 131.
Morán, X. A. G., Lopez-Urrutia, Á., Calvo-Díaz, A., & Li, W. K. (2010). Increasing importance of small phytoplankton in a warmer ocean. Global Change Biology, 16(3), 1137-1144.
Mühlenbruch, M., Grossart, H. P., Eigemann, F., & Voss, M. (2018). Mini-review: Phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environmental Microbiology, 20(8), 2671-2685.
Nelson, C. E., Carlson, C. A., Ewart, C. S., & Halewood, E. R. (2014). Community differentiation and population enrichment of S argasso S Ea bacterioplankton in the euphotic zone of a mesoscale mode-water eddy. Environmental Microbiology, 16(3), 871-887.
O'brien, R. M. (2007). A caution regarding rules of thumb for variance inflation factors. Quality & Quantity, 41(5), 673-690.
Olson, D. B., Hitchcock, G. L., Mariano, A. J., Ashjian, C. J., Peng, G., Nero, R. W., & Podestá, G. P. (1994). Life on the edge: Marine life and fronts. Oceanography, 7(2), 52-60.
Partensky, F., & Garczarek, L. (2010). Prochlorococcus: Advantages and limits of minimalism. Annual Review Marine Science, 2(1), 305-331.
Passow, U., & Carlson, C. A. (2012). The biological pump in a high CO2 world. Marine Ecology Progress Series, 470, 249-271.
Pemberton, K., Rees, A. P., Miller, P. I., Raine, R., & Joint, I. (2004). The influence of water body characteristics on phytoplankton diversity and production in the Celtic Sea. Continental Shelf Research, 24(17), 2011-2028.
Pingree, R., & Griffiths, D. (1978). Tidal fronts on the shelf seas around the British Isles. Journal of Geophysical Research: Oceans, 83(C9), 4615-4622.
Pingree, R., Maddock, L., & Butler, E. (1977). The influence of biological activity and physical stability in determining the chemical distributions of inorganic phosphate, silicate and nitrate. Journal of the Marine Biological Association of the United Kingdom, 57(4), 1065-1073.
Polovina, J. J., Howell, E., Kobayashi, D. R., & Seki, M. P. (2001). The transition zone chlorophyll front, a dynamic global feature defining migration and forage habitat for marine resources. Progress in Oceanography, 49(1-4), 469-483.
Pomeroy, L. R., lB. Williams, P. J., Azam, F., & Hobbie, J. E. (2007). The microbial loop. Oceanography, 20(2), 28-33.
Raes, E. J., Bodrossy, L., Van De Kamp, J., Bissett, A., Ostrowski, M., Brown, M. V., Sow, S. L., Sloyan, B., & Waite, A. M. (2018). Oceanographic boundaries constrain microbial diversity gradients in the South Pacific Ocean. Proceedings of the National Academy of Sciences, 115(35), E8266-E8275.
Richardson, T. L., & Jackson, G. A. (2007). Small phytoplankton and carbon export from the surface ocean. Science, 315(5813), 838-840.
Salter, I., Galand, P. E., Fagervold, S. K., Lebaron, P., Obernosterer, I., Oliver, M. J., Suzuki, M. T., & Tricoire, C. (2015). Seasonal dynamics of active SAR11 ecotypes in the oligotrophic Northwest Mediterranean Sea. The ISME Journal, 9(2), 347-360.
Scales, K. L., Miller, P. I., Hawkes, L. A., Ingram, S. N., Sims, D. W., & Votier, S. C. (2014). On the front line: Frontal zones as priority at-sea conservation areas for mobile marine vertebrates. Journal of Applied Ecology, 51(6), 1575-1583.
Simpson, J., & Hunter, J. (1974). Fronts in the Irish sea. Nature, 250(5465), 404-406.
Sournia, A. (1994). Pelagic biogeography and fronts. Progress in Oceanography, 34(2-3), 109-120.
Spietz, R. L., Williams, C. M., Rocap, G., & Horner-Devine, M. C. (2015). A dissolved oxygen threshold for shifts in bacterial community structure in a seasonally hypoxic estuary. PLoS One, 10(8), e0135731.
Sunagawa, S., Coelho, L. P., Chaffron, S., Kultima, J. R., Labadie, K., Salazar, G., Djahanschiri, B., Zeller, G., Mende, D. R., Alberti, A., & Cornejo-Castillo, F. M. (2015). Structure and function of the global ocean microbiome. Science, 348(6237), 1261359.
Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., Kassabgy, M., Huang, S., Mann, A. J., Waldmann, J., Weber, M., Klindworth, A., Otto, A., Lange, J., Bernhardt, J., Reinsch, C., Hecker, M., Peplies, J., Bockelmann, F. D., … Amann, R. (2012). Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science, 336(6081), 608-611.
Traganza, E. D., Redalije, D. G., & Garwood, R. W. (1987). Chemical flux, mixed layer entrainment and phytoplankton blooms at upwelling fronts in the California coastal zone. Continental Shelf Research, 7(1), 89-105.
Venkatachalam, S., Ansorge, I. J., Mendes, A., Melato, L. I., Matcher, G. F., & Dorrington, R. A. (2017). A pivotal role for ocean eddies in the distribution of microbial communities across the Antarctic circumpolar current. PLoS One, 12(8), e0183400.
Videau, C. (1987). Primary production and physiological state of phytoplankton at the Ushant tidal front (west coast of Brittany, France). Marine Ecololgy Progress Series, 35, 141-151.
Waggitt, J. J., Cazenave, P. W., Howarth, L. M., Evans, P. G., Van der Kooij, J., & Hiddink, J. G. (2018). Combined measurements of prey availability explain habitat selection in foraging seabirds. Biology Letters, 14(8), 20180348.
Walsh, E. A., Kirkpatrick, J. B., Rutherford, S. D., Smith, D. C., Sogin, M., & D'Hondt, S. (2016). Bacterial diversity and community composition from seasurface to subseafloor. The ISME Journal, 10(4), 979-989.
Wang, K., Ye, X., Chen, H., Zhao, Q., Hu, C., He, J., Qian, Y., Xiong, J., Zhu, J., & Zhang, D. (2015). Bacterial biogeography in the coastal waters of northern Zhejiang, East China Sea is highly controlled by spatially structured environmental gradients. Environmental Microbiology, 17(10), 3898-3913.
Wemheuer, B., Güllert, S., Billerbeck, S., Giebel, H.-A., Voget, S., Simon, M., & Daniel, R. (2014). Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiology Ecology, 87(2), 378-389.
Wu, W., Lu, H.-P., Sastri, A., Yeh, Y.-C., Gong, G.-C., Chou, W.-C., & Hsieh, C.-H. (2018). Contrasting the relative importance of species sorting and dispersal limitation in shaping marine bacterial versus protist communities. The ISME Journal, 12(2), 485-494.
Zehr, J. P., & Kudela, R. M. (2011). Nitrogen cycle of the open ocean: From genes to ecosystems. Annual Review Marine Science, 3(1), 197-225.

Auteurs

Nathan G King (NG)

Marine Biological Association of the United Kingdom, The Laboratory, Plymouth, UK.
Centre of Applied Marine Sciences, School of Ocean Sciences, Bangor University, Menai Bridge, UK.

Sophie-B Wilmes (SB)

Centre of Applied Marine Sciences, School of Ocean Sciences, Bangor University, Menai Bridge, UK.

Samuel S Browett (SS)

Environment and Ecosystem Research Centre, School of Science, Engineering and Environment, University of Salford, Salford, UK.
Molecular Ecology Research Group, Eco-Innovation Research Centre, School of Science and Computing, South East Technological University, Waterford, Ireland.

Amy Healey (A)

Department of Life Sciences, Aberystwyth University, Aberystwyth, UK.

Allan D McDevitt (AD)

Department of Natural Resources and Environment, Atlantic Technological University, Galway, Ireland.

Niall J McKeown (NJ)

Department of Life Sciences, Aberystwyth University, Aberystwyth, UK.

Ronan Roche (R)

Centre of Applied Marine Sciences, School of Ocean Sciences, Bangor University, Menai Bridge, UK.

Ilze Skujina (I)

Department of Life Sciences, Aberystwyth University, Aberystwyth, UK.
School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

Dan A Smale (DA)

Marine Biological Association of the United Kingdom, The Laboratory, Plymouth, UK.

Jamie M Thorpe (JM)

Centre of Applied Marine Sciences, School of Ocean Sciences, Bangor University, Menai Bridge, UK.

Shelagh Malham (S)

Centre of Applied Marine Sciences, School of Ocean Sciences, Bangor University, Menai Bridge, UK.

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