Ecological status of Urdaibai Biosphere reserve based on bacterial communities in a small-drainage estuary
Mikel Aguirre
A B , David Abad A C , Aitor Albaina D , Mikel Gutiérrez-Muto A , Jorge Langa A , Marisol Goñi-Urriza E , Maite Orruño F , Inés Arana F , Andone Estonba A and Iratxe Zarraonaindia A G *
+ Author Affiliations
- Author Affiliations
A Department of Genetics, Physical Anthropology and Animal Physiology, Faculty of Science and Technology, University of the Basque Country UPV/EHU, Leioa, Bizkaia, Spain.
B Anbiolab – Anbiotek Biotechnologies S.L., 612, Derio, Bizkaia, Spain.
C Molecular Biology and Microbiology Laboratory, Agricultural Technical Institute of Castilla y León (ITACyL), Valladolid, Spain.
D Department of Zoology and Animal Cell Biology, Faculty of Science and Technology, University of the Basque Country UPV/EHU, Leioa, Bizkaia, Spain.
E CNRS/Université de Pau et des Pays l’Adour, Institut des Sciences Analytiques et de Physico-Chimie pour l’Environnement et les Matériaux, Pau, France.
F Department of Immunology, Microbiology and Parasitology, Faculty of Science and Technology, University of the Basque Country UPV/EHU, Leioa, Bizkaia, Spain.
G IKERBASQUE, Basque Foundation for Science, Bilbao, Spain.
Marine and Freshwater Research 74(8) 651-664 https://doi.org/10.1071/MF22072
Submitted: 15 April 2021 Accepted: 5 April 2023 Published: 5 May 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: The influence of anthropogenic pressures on plankton communities in well-flushed estuaries has been overlooked. Owing to this ecosystem’s short water-residence time, they are foreseen to be mainly composed of microorganisms from neritic–oceanic sources, more resilient to anthropogenic impacts.
Aims: This study characterises the bacterioplankton of Urdaibai, a small-drainage estuary located at a UNESCO biosphere reserve, to unravel its annual dynamic and ecological status.
Methods: Amplicon sequencing was used to assess the euhaline bacterioplankton shifts and microgAMBI index depicted the ecological status of the estuary.
Key results: A differentiated community was identified in upstream waters throughout the year. In addition, organisms commonly associated with faecal waste were detected. The ecological status of the estuary was poor or moderate along the annual cycle, but surprisingly worsened during winter.
Conclusions: The above suggests that the bacterial community dynamic in this well-fluxed small-drainage estuary is more complex than anticipated. Importantly, the analysis of pollution-indicative bacteria proved that the water policy of this estuary needs to be further evaluated.
Implications: The completion of an efficient sewage treatment system for this protected and touristic estuary is strongly recommended. Incorporating bacterial information to its current monitoring system will constitute a useful and valuable tool.
Keywords: 16S rDNA, amplicon sequencing, anthropogenic impact, bacterioplankton, biosphere reserve, drainage estuary, ecological status, spatio-temporal study.
References
Acinas, SG, Antón, J, and Rodríguez-Valera, F (1999). Diversity of free-living and attached bacteria in offshore Western Mediterranean waters as depicted by analysis of genes encoding 16S rRNA. Applied and Environmental Microbiology 65, 514–522.| Diversity of free-living and attached bacteria in offshore Western Mediterranean waters as depicted by analysis of genes encoding 16S rRNA.Crossref | GoogleScholarGoogle Scholar |
Aguirre, M, Abad, D, Albaina, A, Cralle, L, Goñi-Urriza, MS, Estonba, A, and Zarraonaindia, I (2017). Unraveling the environmental and anthropogenic drivers of bacterial community changes in the Estuary of Bilbao and its tributaries. PLoS ONE 12, e0178755.
| Unraveling the environmental and anthropogenic drivers of bacterial community changes in the Estuary of Bilbao and its tributaries.Crossref | GoogleScholarGoogle Scholar |
Albaina, A, Villate, F, and Uriarte, I (2009). Zooplankton communities in two contrasting Basque estuaries (1999–2001): reporting changes associated with ecosystem health. Journal of Plankton Research 31, 739–752.
| Zooplankton communities in two contrasting Basque estuaries (1999–2001): reporting changes associated with ecosystem health.Crossref | GoogleScholarGoogle Scholar |
Apprill, A, McNally, S, Parsons, R, and Weber, L (2015). Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquatic Microbial Ecology 75, 129–137.
| Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton.Crossref | GoogleScholarGoogle Scholar |
Aylagas, E, Borja, A, Tangherlini, M, Dell’anno, A, Corinaldesi, C, Michell, CT, Irigoien, X, Danovaro, R, and Rodriguez-Ezpeleta, N (2017). A bacterial community-based index to assess the ecological status of estuarine and coastal environments. Marine Pollution Bulletin 114, 679–688.
| A bacterial community-based index to assess the ecological status of estuarine and coastal environments.Crossref | GoogleScholarGoogle Scholar |
Bettarel, Y, Bouvier, T, Bouvier, C, Carré, C, Desnues, A, Domaizon, I, Jacquet, S, et al. (2011). Ecological traits of planktonic viruses and prokaryotes along a full-salinity gradient. FEMS Microbiology Ecology 76, 360–372.
| Ecological traits of planktonic viruses and prokaryotes along a full-salinity gradient.Crossref | GoogleScholarGoogle Scholar |
Biddanda, B, Ogdahl, M, and Cotner, J (2001). Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnology and Oceanography 46, 730–739.
| Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters.Crossref | GoogleScholarGoogle Scholar |
Biers, EJ, Sun, S, and Howard, EC (2009). Prokaryotic genomes and diversity in surface ocean waters: interrogating the global ocean sampling metagenome. Applied and Environmental Microbiology 75, 2221–2229.
| Prokaryotic genomes and diversity in surface ocean waters: interrogating the global ocean sampling metagenome.Crossref | GoogleScholarGoogle Scholar |
Bilbao, J, Larreta, J, Franco, J, and Seoane, S (2022). Immediate effect of sewerage improvement on the phytoplankton and physicochemical conditions in the Urdaibai estuary (southeastern Bay of Biscay). Regional Studies in Marine Science 56, 102707.
| Immediate effect of sewerage improvement on the phytoplankton and physicochemical conditions in the Urdaibai estuary (southeastern Bay of Biscay).Crossref | GoogleScholarGoogle Scholar |
Bobrova, O, Kristoffersen, JB, Oulas, A, and Ivanytsia, V (2016). Metagenomic 16S rRNA investigation of microbial communities in the Black Sea estuaries in south-west of Ukraine. Acta Biochimica Polonica 63, 315–319.
| Metagenomic 16S rRNA investigation of microbial communities in the Black Sea estuaries in south-west of Ukraine.Crossref | GoogleScholarGoogle Scholar |
Borja, A (2018). Testing the efficiency of a bacterial community-based index (microgAMBI) to assess distinct impact sources in six locations around the world. Ecological Indicators 85, 594–602.
| Testing the efficiency of a bacterial community-based index (microgAMBI) to assess distinct impact sources in six locations around the world.Crossref | GoogleScholarGoogle Scholar |
Bylak, A, Kukuła, K, Ortyl, B, Hałoń, E, Demczyk, A, Janora-Hołyszko, K, Maternia, J, Szczurowski, L, and Ziobro, J (2022). Small stream catchments in a developing city context: the importance of land cover changes on the ecological status of streams and the possibilities for providing ecosystem services. Science of The Total Environment 815, 151974.
| Small stream catchments in a developing city context: the importance of land cover changes on the ecological status of streams and the possibilities for providing ecosystem services.Crossref | GoogleScholarGoogle Scholar |
Campbell, BJ, and Kirchman, DL (2013). Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. The ISME Journal 7, 210–220.
| Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient.Crossref | GoogleScholarGoogle Scholar |
Campbell, AM, Fleisher, J, Sinigalliano, C, White, JR, and Lopez, JV (2015). Dynamics of marine bacterial community diversity of the coastal waters of the reefs, inlets, and wastewater outfalls of southeast Florida. MicrobiologyOpen 4, 390–408.
| Dynamics of marine bacterial community diversity of the coastal waters of the reefs, inlets, and wastewater outfalls of southeast Florida.Crossref | GoogleScholarGoogle Scholar |
Caporaso, JG, Kuczynski, J, Stombaugh, J, Bittinger, K, Bushman, FD, Costello, EK, Fierer, N, et al. (2010a). QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.
| QIIME allows analysis of high-throughput community sequencing data.Crossref | GoogleScholarGoogle Scholar |
Caporaso, JG, Bittinger, K, Bushman, FD, DeSantis, TZ, Andersen, GL, and Knight, R (2010b). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267.
| PyNAST: a flexible tool for aligning sequences to a template alignment.Crossref | GoogleScholarGoogle Scholar |
Caporaso, JG, Lauber, CL, Walters, WA, Berg-Lyons, D, Huntley, J, Fierer, N, Owens, SM, et al. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6, 1621–1624.
| Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.Crossref | GoogleScholarGoogle Scholar |
Caruso, G, La Ferla, R, Azzaro, M, Zoppini, A, Marino, G, Petochi, T, Corinaldesi, C, et al. (2016). Microbial assemblages for environmental quality assessment: knowledge, gaps and usefulness in the European Marine Strategy Framework Directive. Critical Reviews in Microbiology 42, 883–904.
| Microbial assemblages for environmental quality assessment: knowledge, gaps and usefulness in the European Marine Strategy Framework Directive.Crossref | GoogleScholarGoogle Scholar |
Cearreta A, Monge M, Iriarte E (2006) Seguimiento morfodinámico de la desembocadura del estuario del Oka (Reserva de la Biosfera de Urdaibai). [Morphodynamic monitoring of the mouth of the Oka Estuary (Urdaibai biosphere reserve).] Available at http://www.ingurumena.ejgv.euskadi.eus/contenidos/informe_estudio/ola_mundaka/es_doc/adjuntos/informe_final_mundaka.pdf [In Spanish]
Cloern, JE, and Jassby, AD (2012). Drivers of change in estuarine-coastal ecosystems: discoveries from four decades of study in San Francisco Bay. Reviews of Geophysics 50, RG4001.
| Drivers of change in estuarine-coastal ecosystems: discoveries from four decades of study in San Francisco Bay.Crossref | GoogleScholarGoogle Scholar |
Cloern, JE, Abreu, PC, Carstensen, J, Chauvaud, L, Elmgren, R, Grall, J, Greening, H, et al. (2016). Human activities and climate variability drive fast-paced change across the world’s estuarine-coastal ecosystems. Global Change Biology 22, 513–529.
| Human activities and climate variability drive fast-paced change across the world’s estuarine-coastal ecosystems.Crossref | GoogleScholarGoogle Scholar |
Collado, L, Inza, I, Guarro, J, and Figueras, MJ (2008). Presence of Arcobacter spp. in environmental waters correlates with high levels of fecal pollution. Environmental Microbiology 10, 1635–1640.
| Presence of Arcobacter spp. in environmental waters correlates with high levels of fecal pollution.Crossref | GoogleScholarGoogle Scholar |
Cotano, U, Uriarte, I, and Villate, F (1998). Herbivory of nanozooplankton in polyhaline and euhaline zones of a small temperate estuarine system (Estuary of Mundaka): seasonal variations. Journal of Experimental Marine Biology and Ecology 227, 265–279.
| Herbivory of nanozooplankton in polyhaline and euhaline zones of a small temperate estuarine system (Estuary of Mundaka): seasonal variations.Crossref | GoogleScholarGoogle Scholar |
DeLong, EF, and Karl, DM (2005). Genomic perspectives in microbial oceanography. Nature 437, 336–342.
| Genomic perspectives in microbial oceanography.Crossref | GoogleScholarGoogle Scholar |
Edgar, RC (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
| Search and clustering orders of magnitude faster than BLAST.Crossref | GoogleScholarGoogle Scholar |
Edgar, RC, Haas, BJ, Clemente, JC, Quince, C, and Knight, R (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.
| UCHIME improves sensitivity and speed of chimera detection.Crossref | GoogleScholarGoogle Scholar |
Falkowski, PG, Fenchel, T, and Delong, EF (2008). The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039.
| The microbial engines that drive Earth’s biogeochemical cycles.Crossref | GoogleScholarGoogle Scholar |
Feng, B-W, Li, X-R, Wang, J-H, Hu, Z-Y, Meng, H, Xiang, L-Y, and Quan, Z-X (2009). Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiology Ecology 70, 236–248.
| Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea.Crossref | GoogleScholarGoogle Scholar |
Fortunato, CS, and Crump, BC (2015). Microbial gene abundance and expression patterns across a river to ocean salinity gradient. PLoS ONE 10, e0140578.
| Microbial gene abundance and expression patterns across a river to ocean salinity gradient.Crossref | GoogleScholarGoogle Scholar |
Fortunato, CS, Eiler, A, Herfort, L, Needoba, JA, Peterson, TD, and Crump, BC (2013). Determining indicator taxa across spatial and seasonal gradients in the Columbia River coastal margin. The ISME Journal 7, 1899–1911.
| Determining indicator taxa across spatial and seasonal gradients in the Columbia River coastal margin.Crossref | GoogleScholarGoogle Scholar |
Franco J (1994) Variabilidad espacio-temporal de la biomasa y producción del fitoplancton en el estuario de Urdaibai. PhD thesis, University of the Basque Country, Universidad del País Vasco – Euskal Herriko Unibertsitatea (UPV/EHU), Leioa, Spain.
Galand, PE, Casamayor, EO, Kirchman, DL, and Lovejoy, C (2009). Ecology of the rare microbial biosphere of the Arctic Ocean. Proceedings of the National Academy of Sciences 106, 22427–22432.
| Ecology of the rare microbial biosphere of the Arctic Ocean.Crossref | GoogleScholarGoogle Scholar |
Genitsaris, S, Monchy, S, Breton, E, Lecuyer, E, and Christaki, U (2016). Small-scale variability of protistan planktonic communities relative to environmental pressures and biotic interactions at two adjacent coastal stations. Marine Ecology Progress Series 548, 61–75.
| Small-scale variability of protistan planktonic communities relative to environmental pressures and biotic interactions at two adjacent coastal stations.Crossref | GoogleScholarGoogle Scholar |
Gibbons, SM, Caporaso, JG, Pirrung, M, Field, D, Knight, R, and Gilbert, JA (2013). Evidence for a persistent microbial seed bank throughout the global ocean. Proceedings of the National Academy of Sciences 110, 4651–4655.
| Evidence for a persistent microbial seed bank throughout the global ocean.Crossref | GoogleScholarGoogle Scholar |
Gilbert, JA, Steele, JA, Caporaso, JG, Steinbrück, L, Reeder, J, Temperton, B, Huse, S, et al. (2012). Defining seasonal marine microbial community dynamics. The ISME Journal 6, 298–308.
| Defining seasonal marine microbial community dynamics.Crossref | GoogleScholarGoogle Scholar |
Giovannoni, SJ (2017). SAR11 Bacteria: the most abundant plankton in the oceans. Annual Review of Marine Science 9, 231–255.
| SAR11 Bacteria: the most abundant plankton in the oceans.Crossref | GoogleScholarGoogle Scholar |
Guizien, K, Dupuy, C, Ory, P, Montanié, H, Hartmann, H, Chatelain, M, and Karpytchev, M (2014). Microorganism dynamics during a rising tide: disentangling effects of resuspension and mixing with offshore waters above an intertidal mudflat. Journal of Marine Systems 129, 178–188.
| Microorganism dynamics during a rising tide: disentangling effects of resuspension and mixing with offshore waters above an intertidal mudflat.Crossref | GoogleScholarGoogle Scholar |
Han, D, Shin, H, Lee, J-H, Kang, C-K, Kim, D-G, and Hur, H-G (2022). Phylogenetic diversity and spatiotemporal dynamics of bacterial and microeukaryotic plankton communities in Gwangyang Bay of the Korean Peninsula. Scientific Reports 12, 2980.
| Phylogenetic diversity and spatiotemporal dynamics of bacterial and microeukaryotic plankton communities in Gwangyang Bay of the Korean Peninsula.Crossref | GoogleScholarGoogle Scholar |
Henriques, IS, Alves, A, Tacão, M, Almeida, A, Cunha, Â, and Correia, A (2006). Seasonal and spatial variability of free-living bacterial community composition along an estuarine gradient (Ria de Aveiro, Portugal). Estuarine, Coastal and Shelf Science 68, 139–148.
| Seasonal and spatial variability of free-living bacterial community composition along an estuarine gradient (Ria de Aveiro, Portugal).Crossref | GoogleScholarGoogle Scholar |
Herlemann, DPR, Labrenz, M, Jürgens, K, Bertilsson, S, Waniek, JJ, and Andersson, AF (2011). Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME Journal 5, 1571–1579.
| Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea.Crossref | GoogleScholarGoogle Scholar |
Hicks, GRF (1992). Tidal and diel fluctuations in abundance of meiobenthic copepods on an intertidal estuarine sandbank. Marine Ecology Progress Series 87, 15–21.
| Tidal and diel fluctuations in abundance of meiobenthic copepods on an intertidal estuarine sandbank.Crossref | GoogleScholarGoogle Scholar |
Huete-Stauffer, TM, and Morán, XAG (2012). Dynamics of heterotrophic bacteria in temperate coastal waters: similar net growth but different controls in low and high nucleic acid cells. Aquatic Microbial Ecology 67, 211–223.
| Dynamics of heterotrophic bacteria in temperate coastal waters: similar net growth but different controls in low and high nucleic acid cells.Crossref | GoogleScholarGoogle Scholar |
Hugerth, LW, and Andersson, AF (2017). Analysing microbial community composition through amplicon sequencing: from sampling to hypothesis testing. Frontiers in Microbiology 8, 1561.
| Analysing microbial community composition through amplicon sequencing: from sampling to hypothesis testing.Crossref | GoogleScholarGoogle Scholar |
Iriarte, A, Sarobe, A, and Orive, E (2008). Seasonal variability in bacterial abundance, production and protistan bacterivory in the lower Urdaibai estuary, Bay of Biscay. Aquatic Microbial Ecology 52, 273–282.
| Seasonal variability in bacterial abundance, production and protistan bacterivory in the lower Urdaibai estuary, Bay of Biscay.Crossref | GoogleScholarGoogle Scholar |
Iriarte, A, Aravena, G, Villate, F, Uriarte, I, Ibáñez, B, Llope, M, and Stenseth, NC (2010). Dissolved oxygen in contrasting estuaries of the Bay of Biscay: effects of temperature, river discharge and chlorophyll a. Marine Ecology Progress Series 418, 57–71.
| Dissolved oxygen in contrasting estuaries of the Bay of Biscay: effects of temperature, river discharge and chlorophyll a.Crossref | GoogleScholarGoogle Scholar |
Jeffrey SW, Mantoura RFC (1997) Development of pigment methods for oceanography: SCOR-supported working groups and objectives. In ‘Phytoplankton pigments in oceanography: guidelines to modern methods. Monographs on Oceanographic Methodology’. (Eds SW Jeffrey, RFC Mantoura, SW Wright) pp. 19–36. (UNESCO Publishing)
Jeffries, TC, Schmitz Fontes, ML, Harrison, DP, Van-Dongen-Vogels, V, Eyre, BD, Ralph, PJ, and Seymour, JR (2016). Bacterioplankton dynamics within a large anthropogenically impacted urban estuary. Frontiers in Microbiology 6, 1438.
| Bacterioplankton dynamics within a large anthropogenically impacted urban estuary.Crossref | GoogleScholarGoogle Scholar |
Jiang, X, Zhu, Z, Wu, J, Lian, E, Liu, D, Yang, S, and Zhang, R (2022). Bacterial and protistan community variation across the Changjiang Estuary to the Ocean with multiple environmental gradients. Microorganisms 10, 991.
| Bacterial and protistan community variation across the Changjiang Estuary to the Ocean with multiple environmental gradients.Crossref | GoogleScholarGoogle Scholar |
Joglar, V, Álvarez-Salgado, XA, Gago-Martinez, A, Leao, JM, Pérez-Martínez, C, Pontiller, B, Lundin, D, Pinhassi, J, Fernández, E, and Teira, E (2021). Cobalamin and microbial plankton dynamics along a coastal to offshore transect in the Eastern North Atlantic Ocean. Environmental Microbiology 23, 1559–1583.
| Cobalamin and microbial plankton dynamics along a coastal to offshore transect in the Eastern North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
Kan, J, Evans, SE, Chen, F, and Suzuki, MT (2008). Novel estuarine bacterioplankton in rRNA operon libraries from the Chesapeake Bay. Aquatic Microbial Ecology 51, 55–66.
| Novel estuarine bacterioplankton in rRNA operon libraries from the Chesapeake Bay.Crossref | GoogleScholarGoogle Scholar |
Kirchman, DL, Dittel, AI, Malmstrom, RR, and Cottrell, MT (2005). Biogeography of major bacterial groups in the Delaware Estuary. Limnology and Oceanography 50, 1697–1706.
| Biogeography of major bacterial groups in the Delaware Estuary.Crossref | GoogleScholarGoogle Scholar |
Kostyla, C, Bain, R, Cronk, R, and Bartram, J (2015). Seasonal variation of fecal contamination in drinking water sources in developing countries: a systematic review. Science of The Total Environment 514, 333–343.
| Seasonal variation of fecal contamination in drinking water sources in developing countries: a systematic review.Crossref | GoogleScholarGoogle Scholar |
Kritzberg, ES, Arrieta, JM, and Duarte, CM (2010). Temperature and phosphorus regulating carbon flux through bacteria in a coastal marine system. Aquatic Microbial Ecology 58, 141–151.
| Temperature and phosphorus regulating carbon flux through bacteria in a coastal marine system.Crossref | GoogleScholarGoogle Scholar |
Lanzén, A, Mendibil, I, Borja, A, and Alonso-Sáez, L (2021). A microbial mandala for environmental monitoring: predicting multiple impacts on estuarine prokaryote communities of the Bay of Biscay. Molecular Ecology 30, 2969–2987.
| A microbial mandala for environmental monitoring: predicting multiple impacts on estuarine prokaryote communities of the Bay of Biscay.Crossref | GoogleScholarGoogle Scholar |
Lee, C, Agidi, S, Marion, JW, and Lee, J (2012). Arcobacter in Lake Erie beach waters: an emerging gastrointestinal pathogen linked with human-associated fecal contamination. Applied and Environmental Microbiology 78, 5511–5519.
| Arcobacter in Lake Erie beach waters: an emerging gastrointestinal pathogen linked with human-associated fecal contamination.Crossref | GoogleScholarGoogle Scholar |
Lorenzen, CJ (1967). Determination of chlorophyll and phaeo-pigments: spectrophotometric equations. Limnology and Oceanography 12, 343–346.
| Determination of chlorophyll and phaeo-pigments: spectrophotometric equations.Crossref | GoogleScholarGoogle Scholar |
Lotze, HK, Lenihan, HS, Bourque, BJ, Bradbury, RH, Cooke, RG, Kay, MC, Kidwell, SM, Kirby, MX, Peterson, CH, and Jackson, JBC (2006). Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806–1809.
| Depletion, degradation, and recovery potential of estuaries and coastal seas.Crossref | GoogleScholarGoogle Scholar |
Lê, S, Joss, J, and Husson, F (2008). FactoMineR: an R package for multivariate analysis. Journal of Statistical Software 25, 1–18.
Malmstrom, RR, Cottrell, MT, Elifantz, H, and Kirchman, DL (2005). Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean. Applied and Environmental Microbiology 71, 2979–2986.
| Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
María Trigueros, J, and Orive, E (2000). Tidally driven distribution of phytoplankton blooms in a shallow, macrotidal estuary. Journal of Plankton Research 22, 969–986.
| Tidally driven distribution of phytoplankton blooms in a shallow, macrotidal estuary.Crossref | GoogleScholarGoogle Scholar |
Mason, OU, Canter, EJ, Gillies, LE, Paisie, TK, and Roberts, BJ (2016). Mississippi River plume enriches microbial diversity in the northern Gulf of Mexico. Frontiers in Microbiology 7, 1048.
| Mississippi River plume enriches microbial diversity in the northern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |
Mazard, S, Ostrowski, M, Partensky, F, and Scanlan, DJ (2012). Multi-locus sequence analysis, taxonomic resolution and biogeography of marine Synechococcus. Environmental Microbiology 14, 372–386.
| Multi-locus sequence analysis, taxonomic resolution and biogeography of marine Synechococcus.Crossref | GoogleScholarGoogle Scholar |
McMurdie, PJ, and Holmes, S (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217.
| phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.Crossref | GoogleScholarGoogle Scholar |
Mestre, M, Höfer, J, Sala, MM, and Gasol, JM (2020). Seasonal variation of bacterial diversity along the marine particulate matter continuum. Frontiers in Microbiology 11, 1590.
| Seasonal variation of bacterial diversity along the marine particulate matter continuum.Crossref | GoogleScholarGoogle Scholar |
Monge-Ganuzas, M, Cearreta, A, and Evans, G (2013). Morphodynamic consequences of dredging and dumping activities along the lower Oka estuary (Urdaibai Biosphere Reserve, southeastern Bay of Biscay, Spain). Ocean & Coastal Management 77, 40–49.
| Morphodynamic consequences of dredging and dumping activities along the lower Oka estuary (Urdaibai Biosphere Reserve, southeastern Bay of Biscay, Spain).Crossref | GoogleScholarGoogle Scholar |
Morán, XAG, Ducklow, HW, and Erickson, M (2013). Carbon fluxes through estuarine bacteria reflect coupling with phytoplankton. Marine Ecology Progress Series 489, 75–85.
| Carbon fluxes through estuarine bacteria reflect coupling with phytoplankton.Crossref | GoogleScholarGoogle Scholar |
Newton, RJ, Huse, SM, Morrison, HG, Peake, CS, Sogin, ML, and McLellan, SL (2013). Shifts in the microbial community composition of gulf coast beaches following beach oiling. PLoS ONE 8, e74265.
| Shifts in the microbial community composition of gulf coast beaches following beach oiling.Crossref | GoogleScholarGoogle Scholar |
Nydahl, A, Panigrahi, S, and Wikner, J (2013). Increased microbial activity in a warmer and wetter climate enhances the risk of coastal hypoxia. FEMS Microbiology Ecology 85, 338–347.
| Increased microbial activity in a warmer and wetter climate enhances the risk of coastal hypoxia.Crossref | GoogleScholarGoogle Scholar |
Orive, E, Iriarte, A, De Madariaga, I, and Revilla, M (1998). Phytoplankton blooms in the Urdaibai estuary during summer: physico-chemical conditions and taxa involved. Oceanologica Acta 21, 293–305.
| Phytoplankton blooms in the Urdaibai estuary during summer: physico-chemical conditions and taxa involved.Crossref | GoogleScholarGoogle Scholar |
Paulson, JN, Stine, OC, Bravo, HC, and Pop, M (2013). Differential abundance analysis for microbial marker-gene surveys. Nature Methods 10, 1200–1202.
| Differential abundance analysis for microbial marker-gene surveys.Crossref | GoogleScholarGoogle Scholar |
Pendleton, LH, Thebaud, O, Mongruel, RC, and Levrel, H (2016). Has the value of global marine and coastal ecosystem services changed? Marine Policy 64, 156–158.
| Has the value of global marine and coastal ecosystem services changed?Crossref | GoogleScholarGoogle Scholar |
Price, PB, and Sowers, T (2004). Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proceedings of the National Academy of Sciences of the United States of America 101, 4631–4636.
| Temperature dependence of metabolic rates for microbial growth, maintenance, and survival.Crossref | GoogleScholarGoogle Scholar |
Pringault, O, Bouvy, M, Carré, C, Mejri, K, Bancon-Montigny, C, Gonzalez, C, Leboulanger, C, Hlaili, AS, and Goñi-Urriza, M (2021). Chemical contamination alters the interactions between bacteria and phytoplankton. Chemosphere 278, 130457.
| Chemical contamination alters the interactions between bacteria and phytoplankton.Crossref | GoogleScholarGoogle Scholar |
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J, et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.
| The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.Crossref | GoogleScholarGoogle Scholar |
Rasmussen, AN, Damashek, J, Eloe-Fadrosh, EA, and Francis, CA (2021). In-depth spatiotemporal characterization of planktonic archaeal and bacterial communities in North and South San Francisco Bay. Microbial Ecology 81, 601–616.
| In-depth spatiotemporal characterization of planktonic archaeal and bacterial communities in North and South San Francisco Bay.Crossref | GoogleScholarGoogle Scholar |
Revilla, M, Iriarte, A, Madariaga, I, and Orive, E (2000). Bacterial and phytoplankton dynamics along a trophic gradient in a shallow temperate estuary. Estuarine, Coastal and Shelf Science 50, 297–313.
| Bacterial and phytoplankton dynamics along a trophic gradient in a shallow temperate estuary.Crossref | GoogleScholarGoogle Scholar |
Ruiz, A, Franco, J, and Orive, E (1994). Suspended particulate matter dynamics in the shallow mesotidal urdaibai estuary (Bay of Biscay, Spain). Netherlands Journal of Aquatic Ecology 28, 309–316.
| Suspended particulate matter dynamics in the shallow mesotidal urdaibai estuary (Bay of Biscay, Spain).Crossref | GoogleScholarGoogle Scholar |
Selje, N, and Simon, M (2003). Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany. Aquatic Microbial Ecology 30, 221–237.
| Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany.Crossref | GoogleScholarGoogle Scholar |
Seymour, JR, Amin, SA, Raina, J-B, and Stocker, R (2017). Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nature Microbiology 2, 17065.
| Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships.Crossref | GoogleScholarGoogle Scholar |
Shibata, T, Solo-Gabriele, HM, Fleming, LE, and Elmir, S (2004). Monitoring marine recreational water quality using multiple microbial indicators in an urban tropical environment. Water Research 38, 3119–3131.
| Monitoring marine recreational water quality using multiple microbial indicators in an urban tropical environment.Crossref | GoogleScholarGoogle Scholar |
Trigueros, JM, and Orive, E (2001). Seasonal variations of diatoms and dinoflagellates in a shallow, temperate estuary, with emphasis on neritic assemblages. Hydrobiologia 444, 119–133.
| Seasonal variations of diatoms and dinoflagellates in a shallow, temperate estuary, with emphasis on neritic assemblages.Crossref | GoogleScholarGoogle Scholar |
Vaqué, D, Guadayol, Ò, Peters, F, Felipe, J, Malits, A, and Pedrós-Alió, C (2009). Differential response of grazing and bacterial heterotrophic production to experimental warming in Antarctic waters. Aquatic Microbial Ecology 54, 101–112.
| Differential response of grazing and bacterial heterotrophic production to experimental warming in Antarctic waters.Crossref | GoogleScholarGoogle Scholar |
Vargas, CA, Martínez, RA, Cuevas, LA, Pavez, MA, Cartes, C, González, HE, Escribano, R, et al. (2007). The relative importance of microbial and classical food webs in a highly productive coastal upwelling area. Limnology and Oceanography 52, 1495–1510.
| The relative importance of microbial and classical food webs in a highly productive coastal upwelling area.Crossref | GoogleScholarGoogle Scholar |
Villate, F (1997). Tidal influence on zonation and occurrence of resident and temporary zooplankton in a shallow system (Estuary of Mundaka, Bay of Biscay). Scientia Marina 61, 173–188.
Wang, H, Chen, F, Zhang, C, Wang, M, and Kan, J (2021). Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay. Environmental Microbiome 16, 22.
| Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay.Crossref | GoogleScholarGoogle Scholar |
Wu, L, Ning, D, Zhang, B, Li, Y, Zhang, P, Shan, X, Zhang, Q, et al. (2019). Global diversity and biogeography of bacterial communities in wastewater treatment plants. Nature Microbiology 4, 1183–1195.
| Global diversity and biogeography of bacterial communities in wastewater treatment plants.Crossref | GoogleScholarGoogle Scholar |
Wurtsbaugh, WA, Paerl, HW, and Dodds, WK (2019). Nutrients, eutrophication and harmful algal blooms along the freshwater to marine continuum. WIREs Water 6, e1373.
| Nutrients, eutrophication and harmful algal blooms along the freshwater to marine continuum.Crossref | GoogleScholarGoogle Scholar |
Zhang, J, Kobert, K, Flouri, T, and Stamatakis, A (2014). PEAR: a fast and accurate Illumina paired-end read merger. Bioinformatics 30, 614–620.
| PEAR: a fast and accurate Illumina paired-end read merger.Crossref | GoogleScholarGoogle Scholar |
Zhao, J, Peng, W, Ding, M, Nie, M, and Huang, G (2021). Effect of water chemistry, land use patterns, and geographic distances on the spatial distribution of bacterioplankton communities in an anthropogenically disturbed riverine ecosystem. Frontiers in Microbiology 12, 633993.
| Effect of water chemistry, land use patterns, and geographic distances on the spatial distribution of bacterioplankton communities in an anthropogenically disturbed riverine ecosystem.Crossref | GoogleScholarGoogle Scholar |
Zhou, L, Huang, S, Gong, J, Xu, P, and Huang, X (2022). 500 metagenome-assembled microbial genomes from 30 subtropical estuaries in South China. Scientific Data 9, 310.
| 500 metagenome-assembled microbial genomes from 30 subtropical estuaries in South China.Crossref | GoogleScholarGoogle Scholar |
