Structure and dynamics of bacterioplankton from four Pampean shallow lakes of the Salado River basin (Buenos Aires, Argentina)

Authors

  • Guillermina Nuozzi Departamento de Ciencias Básicas y Experimentales, Universidad Nacional del Noroeste de la Provincia de Buenos Aires (UNNOBA). Junín, Argentina. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires (CITNOBA)-UNNOBA-UNSAdA-CONICET
  • Camila Seoane Rocha Cátedra de Citología, Histología y Embriología, Facultad de Ciencias Médicas, Universidad Nacional de La Plata (UNLP). Buenos Aires, Argentina
  • Mara Sagua Departamento de Ciencias Básicas y Experimentales, Universidad Nacional del Noroeste de la Provincia de Buenos Aires (UNNOBA). Junín, Argentina. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires (CITNOBA)-UNNOBA-UNSAdA-CONICET
  • M. Eugenia Llames Instituto Tecnológico de Chascomús (INTECH), Universidad Nacional de San Martín (UNSAM)-Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Chascomús, Buenos Aires, Argentina
  • Paula Huber Instituto Nacional de Limnología (INALI, CONICET-UNL). Santa Fe, Argentina
  • Sebastián Metz Université de Bretagne Occidentale, CNRS, IRD, Ifremer, LEMAR. Plouzané, France
  • Leonardo Lagomarsino Instituto Tecnológico de Chascomús (INTECH), Universidad Nacional de San Martín (UNSAM)-Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Chascomús, Buenos Aires, Argentina
  • M. Romina Schiaffino Departamento de Ciencias Básicas y Experimentales, Universidad Nacional del Noroeste de la Provincia de Buenos Aires (UNNOBA). Junín, Argentina. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires (CITNOBA)-UNNOBA-UNSAdA-CONICET

DOI:

https://doi.org/10.25260/EA.22.32.2.0.1811

Keywords:

planktonic bacteria, temporal dynamic, turbid-clear regime, illumina

Abstract

Bacterioplankton is an essential component for the functioning of aquatic ecosystems and has a profound impact on the water quality of the aquatic environments. It is therefore important to increase knowledge about its dynamics and genetic diversity. The main objectives of this work were to evaluate the structure and dynamics of bacterioplankton from four Pampean shallow lakes located in the upper (Gómez and Carpincho) and lower (Chascomús and El Triunfo) basins of the Salado River, as well as to determine the influence of environmental factors on these communities. To achieve this, seasonal samplings were performed during one year (January 2015-January 2016), in which main limnological variables were determined and the structure of bacterioplankton was analyzed by means of Illumina next-generation amplicon sequencing of the 16S rRNA gene. Bacterioplankton diversity indices were significantly higher in shallow lakes from the upper basin relative to those of the lower basin. Bacterioplankton richness was significantly lower in the clear-regime and disconnected shallow lake (El Triunfo) than in the turbid-regime and connected shallow lakes (Gómez, Carpincho and Chascomús). Bacterioplankton composition differed between all shallow lakes, except between the nearby and interconnected shallow lakes (Gómez and Carpincho). Environmental variables, such as total phosphorus, conductivity and Secchi depth, influenced the bacterioplankton composition in the studied lakes. Similarity in the bacterioplankton composition increased significantly with higher environmental similarity between lakes and decreased with spatial distance between them. Our results showed the bacterioplankton structure of the studied lakes was ruled by environmental and spatial factors. The bacterial structure varied between basins, and also between systems with different regimes and/or connections to the river.

References

Adamovich, B. V., T. V. Zhukova, T. M. Mikheeva, R. Z. Kovalevskaya, and E. V. Luk’yanova. 2016. Long-term variations of the trophic state index in the Narochanskie Lakes and its relation with the major hydroecological parameters. Water Resources 43(5):809-817. https://doi.org/10.1134/S009780781605002X.

Allende, L., G. Tell, H. Zagarese, A. Torremorell, G. Pérez, J. Bustingorry, R. Escaray, and I. Izaguirre. 2009. Phytoplankton and primary production in clear-vegetated, inorganic-turbid, and algal-turbid shallow lakes from the pampa plain (Argentina). Hydrobiology 624(1):45-60. https://doi.org/10.1007/s10750-008-9665-9.

Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J Mol Biol 215(3):403-10. https://doi.org/10.1016/S0022-2836(05)80360-2.

APHA (American Public Health Association). 1992. Standard Methods for the Examination of Water and Wastewater. Washington D.C.

APHA (American Public Health Association). 2005. Standard Methods for the Examination of Waters and Wastewater, 21st ed. Washington D.C.

Barbosa da Costa, N., V. Fugère, M. P. Hébert, C. C. Y. Xu, R. D. H. Barrett, B. E. Beisner, G. Bell, V. Yargeau, G. F. Fussmann, A. González, and B. J. Shapiro. 2021. Resistance, resilience, and functional redundancy of freshwater bacterioplankton communities facing a gradient of agricultural stressors in a mesocosm experiment. Molecular Ecology 30(19):4771-4788. https://doi.org/10.1111/mec.16100.

Bazzuri, M. E., N. A. Gabellone, and L. C. Solari. 2018. The effects of hydraulic works and wetlands function in the Salado-River basin (Buenos Aires, Argentina). Environmental Monitoring and Assessment 190(2):99. https://doi.org/10.1007/s10661-017-6448-7.

Bettolli, M. L., W. M. Vargas, and O. C Penalba. 2009. Soya bean yield variability in the Argentine Pampas in relation to synoptic weather types: monitoring implications. Meteorological Applications 16:501-511. https://doi.org/10.1002/met.148.

Burgos, J. J., and A. L. Vidal. 1951. The climates of the Argentine Republic according to the new Thornthwaite classification. Annals of the Association of American Geographers 41(3):237-263. https://doi.org/10.2307/2561011.

Cabrini, S. M., S. I. Portela, P. B. Cano, P. B., and D. A. López. 2019. Heterogeneity in agricultural land use decisions in Argentine Rolling Pampas: The effects on environmental and economic indicators. Cogent Environmental Science 5(1):1667709. https://doi:10.1080/23311843.2019.1667709.

Callahan, B. J., P. J. McMurdie, M. J. Rosen, A. W. Han, A. J. A. Johnson, and S. P. Holmes. 2016. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13(7):581-3. https://doi.org/10.1038/nmeth.3869.

Castro Berman, M., M. E. Llames, P. Minotti, P. Fermani, M. V. Quiroga, M. A. Ferraro, S. Metz, and H. E. Zagarese. 2020. Field evidence supports former experimental claims on the stimulatory effect of glyphosate on picocyanobacteria communities. Science of The Total Environment 701:134601. https://doi.org/10.1016/j.scitotenv.2019.134601.

Castro Berman, M., D. J. G. Marino, M. V. Quiroga, and H. Zagarese. 2018. Occurrence and levels of glyphosate and AMPA in shallow lakes from the Pampean and Patagonian regions of Argentina. Chemosphere 200:513-522. https://doi.org/10.1016/j.chemosphere.2018.02.103.

De Figueiredo, D. R., M. J. Pereira, and A. Correia 2010. Seasonal modulation of bacterioplankton community at a temperate eutrophic shallow lake. World Journal of Microbiology and Biotechnology 26:1067-1077. https://doi.org/10.1007/s11274-009-0272-3.

Diovisalvi, N., V. Y. Bohn, M. C. Piccolo, G. M. E Perillo, C. R. M. Baigún, and H. E. Zagarese. 2015. Shallow lakes from the Central Plains of Argentina: an overview and worldwide comparative analysis of their basic limnological features. Hydrobiologia 752:5-20. https://doi.org/10.1007/s10750-014-1946-x.

Dolan, J. R. 2005. Biogeography of aquatic microbes. Aquatic Microbial Ecology 41:39-48. http://doi.org/10.3354/ame041039.

Dray, S., and A. B. Dufour. 2007. The ade4 Package: Implementing the Duality Diagram for Ecologists. Journal of Statistical Software 22(4):1-20. https://doi.org/10.18637/jss.v022.i04.

Ducklow, H. 2008. Microbial services: challenges for microbial ecologists in a changing world. Aquat Microb Ecol 53:13-19. https://doi.org/10.3354/ame01220.

Edgar, R. C., and H. Flyvbjerg. 2015. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31(21):3476-82. https://doi.org/10.1093/bioinformatics/btv401.

Fenchel, T. 2008. The microbial loop-25 years later. Journal of Experimental Marine Biology and Ecology 366:99-103. https://doi.org/10.1016/j.jembe.2008.07.013.

Fermani, P., A. Torremorell, L. Lagomarsino, R. Escaray, F. Unrein, and G. Pérez. 2015. Microbial abundance patterns along a transparency gradient suggest a weak coupling between heterotrophic bacteria and flagellates in eutrophic shallow Pampean lakes. Hydrobiologia 752:103-123. https://doi.org/10.1007/s10750-014-2019-x.

Fernández Zenoff, V., F. Siñeriz, and M. E. Farías. 2006. Diverse Responses to UV‐B Radiation and Repair Mechanisms of Bacteria Isolated from High‐Altitude Aquatic Environments. Applied Environmental Microbiology 72(12):7857‐7863. https://doi.org/10.1128/AEM.01333-06.

Fisher, S. G., N. B. Grimm, E. Martí, R. M Holmes, and J. B. Jones. 1998. Material spiraling in stream corridors: a telescoping ecosystem model. Ecosystems 1(1):19-34. https://doi.org/10.1007/s100219900003.

Gabellone, N. A., L. C. Solari, and M. C. Claps. 2001. Planktonic and physicochemical dynamics of a markedly fluctuating backwater pond associated with a lowland river (Salado River, Buenos Aires, Argentina). Lakes and Reservoirs: Research and Management 6:133-142. https://doi.org/10.1046/j.1440-1770.2001.00130.x.

Gabellone, N. A., R. Sarandón, and C. Claps. 2003. Caracterización y zonificación ecológica de la Cuenca del Río Salado. En O. C. Maiola, N. A. Gabellone and M. A. Hernández (eds.). Inundaciones en la región pampeana. 1ra edición. Editorial de la Universidad Nacional de La Plata, La Plata, Argentina.

Gabellone, N., M. C. Claps, L. C. Solari, and N. C. Neschuk. 2005. Nutrients, conductivity and plankton in a landscape approach to a Pampean saline lowland river (Salado River, Argentina). Biogeochemistry 75:455-477. https://doi.org/10.1007/s10533-005-3273-9.

Gabellone, N. A., L. Solari, M. Claps, and N. Neschuk. 2008. Chemical classification of the water in a lowland river basin (Salado River, Buenos Aires, Argentina) affected by hydraulic modifications. Environmental Geology 53:1353-1363. https://doi.org/10.1007/s00254-007-0745-3.

Gabellone, N. A., M. C. Claps, D. C. Ardohain, A. Dippolito, M. E. Bazurri, and L. C. Solari. 2014. Trophic and structural relationship between zoo- and phytoplankton in a saline lowland river (Argentina): a short-time-scale analysis. Fundamental and Applied Limnology 184(4):307-327. https://doi.org/10.1127/1863-9135/2014/0643.

Goslee, S. C., and D. L. Urban. 2007. The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22(7):1-19. https://doi.org/10.18637/jss.v022.i07.

Grosman, F. 2008. Espejos en la llanura: Nuestras lagunas de la región pampeana. Primera edición. Tandil. Univ. Nacional del Centro de la Provincia de Buenos Aires.

Hébert, M. P., V. Fugère, and A. González. 2018. The overlooked impact of rising glyphosate use on phosphorus loading in agricultural watersheds. Frontiers in Ecology and the Environment 17(1):48-56. https://doi.org/10.1002/fee.1985.

Herlemann, D. P., M. Labrenz, K. Jürgens, S. Bertilsson, J. J. Waniek, and A. F. Andersson. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME journal 5:1571-1579. https://doi.org/10.1038/ismej.2011.41.

Huber, P., N. Diovisalvi, M. Ferraro, S. Metz, L. Lagomarsino, M. E. Llames, M. Royo-Llonch, J. Bustingorry, R. Escaray, S. G. Acinas, J. M. Gasol, and F. Unrein. 2017. Phenotypic plasticity in freshwater picocyanobacteria. Environmental Microbiology 19(3):1120-1133. https://doi.org/10.1111/1462-2920.13638.

Izaguirre, I., M. L. Sánchez, M. R. Schiaffino, I. O’Farrell, P. Huber, N. Ferrer, J. Zunino, L. Lagomarsino, and Miguel Mancini. 2015. Which environmental factors trigger the dominance of phytoplankton species across a moisture gradient of shallow lakes Hydrobiologia 752(1):47-64. https://doi.org/10.1007/s10750-016-2951-z.

Izaguirre, I., and A. Vinocur. 1994. Algal assemblages from shallow lakes of the Salado River Basin (Argentina). Hydrobiologia 289:57-64. https://doi.org/10.1007/BF00007408.

Kraemer, S. A., N. Barbosa da Costa, B. J. Shapiro, M. Fradette, Y. Huot, and D. A. Walsh. 2020. A large-scale assessment of lakes reveals a pervasive signal of land use on bacterial communities. The ISME Journal 14:3011-3023. https://doi.org/10.1038/s41396-020-0733-0.

Lake, P. S. 2003. Ecological effects of perturbation by drought in flowing waters. Freshwater Biology 48(7):1161-1172. https://doi.org/10.1046/j.1365-2427.2003.01086.x.

Legendre, P., and L. Legendre. 1998. Numerical Ecology. Second Edition. Elsevier, Amsterdam.

Legendre, P., and E. Gallagher. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129:271-280. https://doi.org/10.1007/s004420100716.

Llames, M. 2011. Diversidad y ecología de las comunidades microbiológicas de las lagunas pampeanas. Tesis doctoral. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina. Pp. 159.

Llames, M. E., P. A del Giorgio, H. Zagarese, M. Ferraro, and I. Izaguirre. 2013. Alternative states drive the patterns in the bacterioplankton composition in shallow Pampean lakes (Argentina). Environmental Microbiology Reports 5(2):310-321. https://doi:10.1111/1758-2229.12020.

Llames, M. E., P. Huber, S. Metz, and F. Unrein. 2017. Interplay between stochastic and deterministic processes in the maintenance of alternative community states in Verrucomicrobia-dominated shallow lakes. FEMS Microbiology Ecology 93(7):1-10. https://doi.org/10.1093/femsec/fix077.

Logue, J. B., and E. Lindström. 2008. Biogeography of bacterioplankton in inland waters. Freshwater Reviews 1:99-114. https://doi.org/10.1608/FRJ-1.1.9.

Malvárez, A. I., and R. F. Bó. 2004. Documentos del Curso Taller: Bases ecológicas para la clasificación e inventario de humedales en Argentina, Buenos Aires. Primera edición. Buenos Aires. URL: lac.wetlands.org/caso/inventario-de-humedales.

Mantel, N., and R. S. Valand. 1970. A technique of nonparametric multivariate analysis. Biometrics 26(3):547-558. https://doi.org/10.2307/2529108.

Marker, A. F. H., E. A. Nusch, H. Rai, and B. Riemann. 1980. The measurement of photosynthetic pigments in freshwater and standardization of methods: conclusions and recommendations. Archiv für Hydrobiologie Behandlung Ergebnisse der Limnologie 14:91-106.

Martin, M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17(1):10-12. https://doi.org/10.14806/ej.17.1.200.

Martiny, J. B. H., B. J. M. Bohannan, J. H. Brown, R. K. Colwell, J. A. Fuhrman, J. L. Green, M. C. Horner-Devine, M. Kane, J. Adams Krumins, C. R. Kuske, P. J. Morin, S. Naeem, L. Ovreås, A.-L. Reysenbach, V. H. Smith, and J. T. Staley. 2006. Microbial biogeography: putting microorganisms on the map. Nature Reviews Microbiology 4:102-112. https://doi.org/10.1038/nrmicro1341.

MEA (Millennium Ecosystem Assessment). 2005. Ecosystems and human well-being: Wetlands and water synthesis. World Resources Institute, Washington D.C.

Morin, P. J., and J. McGrady-Steed. 2004. Biodiversity and ecosystem functioning in aquatic microbial systems: a new analysis of temporal variation and species richness predictability relations. Oikos 104:458-466. https://doi.org/10.1111/J.0030-1299.2004.13256.X.

Muylaert, K., K. Van der Gucht, N. Vloemans, L. De Meester, M. Gillis, and W. Vyverman. 2002. Relationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes. Applied and Environmental Microbiology 68(10):4740-4750. https://doi.org/10.1128/AEM.68.10.4740-4750.2002.

Newton, R. J., S. E Jones, A. Eiler, K. D. McMahon, and S. Bertilsson. 2011. A guide to the natural history of freshwater lake bacteria. Microbiology and Molecular Biology Reviews 75(1):14-49. https://doi.org/10.1128/MMBR.00028-10.

O’Farrell, I., C. Motta, M. Forastier, W. Polla, S. Otaño, N. Meichtry, M. Devercelli, and R. Lombardo. 2019. Ecological meta-analysis of the bloom-forming planktonic Cyanobacteria in Argentina. Harmful Algae 83:1-13. https://doi.org/10.1016/j.hal.2019.01.004.

O´Farrell, I., M. L. Sánchez, M. R. Schiaffino, I. Izaguirre, P. Huber, L. Lagomarsino, and L. Yema. 2021. Human impacted shallow lakes in the Pampean plain are ideal hosts for cyanobacterial harmful algae. Environmental Pollution 288:117747. https://doi.org/10.1016/j.envpol.2021.117747.

Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, P. Solymos, M. Henry, H. Stevens, E. Szoecs, H. Wagner, M. Barbour, M. Bedward, B. Bolker, D. Borcard, G. Carvalho, M. Chirico, M. De Caceres, S. Durand, H. B. Antoniazi Evangelista, R. FitzJohn, M. Friendly, B. Furneaux, G. Hannigan, M. O. Hill, L. Lahti, D. McGlinn, M.-H. Ouellette, E. Ribeiro Cunha, T. Smith, A. Stier, C. J. F. Ter Braak, and J. Weedon. 2017. Vegan: Community Ecology Package. R package version 2.0-2. URL: cran.r-project.org/package=vegan.

Pasqualetti, C., F. Szokoli, L. Rindi, G. Petroni, and M. Schrallhammer. 2020. The Obligate Symbiont Candidatus Megaira polyxenophila Has Variable Effects on the Growth of Different Host Species. Frontiers in Microbiology 11. https://doi.org/10.3389/fmicb.2020.01425.

Prosser, J. I., B. J. Bohannan, T. P Curtis, R. J. Ellis, M. K. Firestone, R. P. Freckleton, J. L. Green, L. E. Green, K. Killham, J. J. Lennon, A. M. Osborn, M. Solan, C. J. van der Gast, and J. P. W. Young. 2007. The role of ecological theory in microbial ecology. Nature Reviews Microbiology 5(5):384-392. https://doi.org/10.1038/nrmicro1643.

Quast, C., E. Pruesse, P. Yilmaz, J. Gerken, T. Schweer, P. Yarza, J. Peplies, and F. O. Glöckner. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41:D590-D596. https://doi.org/10.1093/nar/gks1219.

Quiroga, M. P. 2020. Diversidad de bacterias planctónicas en lagunas pampeanas utilizadas con fines recreativos. Tesis de grado. Facultad de Ciencias Exactas. Universidad Nacional de La Plata, Buenos Aires, Argentina. Pp. 66.

Quirós, R. 2000. La eutrofización de las aguas continentales en Argentina. I Reunión de la Red Temática sobre Eutrofización de Lagos y Embalses. Subprograma XVII. Cooperación Iberoamericana. Ciencia y tecnología para el desarrollo (CYTED). Mar del Plata, Argentina.

Quirós, R. 2005. La ecología de las lagunas de las Pampas. Investigación y Ciencia 1-13. URL: tinyurl.com/n7dpf98r.

Quirós, R., and E. Drago. 1999. The environmental state of Argentinean lakes: An overview. Lakes and Reservoirs: Research and Management 4:55-64. https://doi.org/10.1046/j.1440-1770.1999.00076.x.

Quirós, R., J. J. Rosso, A. M. Rennella, A. Sosnovsky, and M. B. Boveri. 2002a. Análisis del estado trófico de las lagunas pampeanas (Argentina). Interciencia 27(11):584-591. URL: tinyurl.com/bp6cb6vh.

Quirós, R., A. M, Rennella, M. B Boveri, J. J. Rosso, and A. Sosnovsky. 2002b. Factores que afectan la estructura y el funcionamiento de las lagunas pampeanas. Ecología Austral 12(2):175-185.

Quirós, R., M. B. Boveri, C. A. Petracci, A. M. Renella, J. J. Rosso, A. Sosnovsky, and von

H. T. Bernard. 2006. Los efectos de la agriculturización del humedal pampeano sobre la eutrofización de sus lagunas. Pp. 1-16 en J. G. Tundisi, T. Matsumura-Tundisi and C. Sidagis Galli (eds.). Eutrofização na América do Sul: Causas, conseqüências e tecnologias de gerenciamento e controle. Instituto Internacional de Ecologia, Instituto Internacional de Ecologia e Gerenciamento Ambiental, Academia Brasileira de Ciências, Conselho Nacional de Desenvolvimento Científico e Tecnológico, InterAcademy Panel on International Issues, InterAmerican Network of Academies of Sciences.

R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. 2018. URL: R-project.org.

Rennella, A. M., and R. Quirós. 2006. The effects of hydrology on plankton biomass in shallow lakes of the Pampa Plain. Hydrobiologia 556:181-191. https://doi.org/10.1007/s10750-005-0318-y.

Ringuelet, R. A., A. Salibián, E. Clavérie, and S. Ilhero. 1967. Limnología química de las lagunas pampásicas (Provincia de Buenos Aires). Physis 27:201-221.

Rosso, J. J. 2008. Relación entre la abundancia y estructura de la comunidad de peces y el régimen hidrológico, en lagunas de la alta cuenca del Río Salado. Tesis doctoral. Facultad de Agronomía. Universidad de Buenos Aires, Buenos Aires, Argentina. Pp. 115

Sánchez, M. L., L. Lagomarsino, L. Allende, and I. Izaguirre. 2014. Changes in the phytoplankton structure in a Pampean shallow lake in the transition from a clear to a turbid regime. Hydrobiologia, 752(1):65-76. https://doi.org/10.1007/s10750-014-2010-6.

Sánchez, M. L., M. R. Schiaffino, M. Graziano, P. Huber, L. Lagomarsino, P. Minotti, H. Zagarese, and I. Izaguirre. 2021. Effect of land use on the phytoplankton community of Pampean shallow lakes of the Salado River basin (Buenos Aires Province, Argentina). Aquatic Ecology 55:417-435. https://doi.org/10.1007/s10452-021-09835-8.

Sánchez, L. M., M. R. Schiaffino, H. Pizarro, and I. Izaguirre. 2015. Periphytic and planktonic bacterial community structure in turbid and clear shallow lakes of the Pampean Plain (Argentina): a CARD-FISH approach. Latin American Journal of Aquatic Research 43(4):662-674. https://doi.org/10.3856/vol43-issue4-fulltext-5.

Savicky, P. 2014. Pspearman: Spearman’s Rank Correlation Test. URL: CRAN.R-project.org/package=pspearman.

Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss, and E. Jeppesen. 1993. Alternative equilibria in shallow lakes, Trends in Ecology and Evolution 8(8):275-279. https://doi.org/10.1016/0169-5347(93)90254-M.

Schiaffino, M. R., N. Diovisalvi, D. M. Molina, P. Fermani, C. Li Puma, L. Lagomarsino, M. V. Quiroga, and G. L. Pérez. 2019. Microbial food-web components in two hypertrophic human-impacted Pampean shallow lakes: interactive effects of environmental, hydrological, and temporal drivers. Hydrobiologia 830:255-276. https://doi.org/10.1007/s10750-018-3874-7.

Schiaffino, M. R., P. Huber, M. Sagua, C. A Sabio, Y. García, and M. Reissig. 2020. Covariation patterns of phytoplankton and bacterioplankton in hypertrophic shallow lakes. FEMS Microbiology Ecology 96(11):fiaa161. https://doi.org/10.1093/femsec/fiaa161.

Seoane Rocha, C. 2018. Estructura y dinámica del bacterioplancton en lagunas ubicadas en la cuenca superior e inferior del río Salado. Tesis de grado. Escuela de Ciencias Agrarias, Naturales y Ambientales. Universidad Nacional del Noroeste de la Provincia de Buenos Aires. Pp. 67.

Sierra, E. M., R. Hurtado, L. Spescha, I. Barnatan, and C. Messina. 1994. Corrimiento de las isoyetas semestrales medias decenales (1941-1990) en la región pampeana. Revista Facultad de Agronomía 15(2-3):137-143. URL: tinyurl.com/3asz3s5k.

Simões, N. R., F. A Lansac-Tôha, and C. Bonecker. 2013. Drought disturbances increase temporal variability of zooplankton community structure in floodplains. International Review of Hydrobiology 98:24-33. https://doi.org/10.1002/iroh.201201473.

Steven, B., S. E. Dowd, K. H. Schulmeyer, and N. L. Ward. 2011. Phylum-targeted pyrosequencing reveals diverse planctomycete populations in a eutrophic lake. Aquatic Microbial Ecology 64:41-49. https://doi.org/10.3354/ame01507.

Taranu, Z. E., and I. Gregory-Eaves. 2008. Quantifying relationships among phosphorus, agriculture, and lake depth at an interregional scale. Ecosystems 11:715-725. https://doi.org/10.1007/s10021-008-9153-0.

Tong Y., G. Lin, X. Ke, F. Liu, G. Zhu, G. Gao, and J. Shen. 2005. Comparison of microbial community between two shallow freshwater lakes in middle Yangtze basin, East China. Chemosphere 60(1):85-92. https://doi.org/10.1016/j.chemosphere.2005.01.037.

Van der Gucht, K., K. Sabbe, L. De Meester, N. Vloemans, G. Zwart, M. Gillis, and W. Vyverman. 2001. Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. Environmental Microbiology 3(11):680-690. http://doi.org/10.1046/j.1462-2920.2001.00242.x.

Viglizzo, E. F., F. Lértora, A. J. Pordomingo, J. N. Bernardos, Z. E. Roberto, H. Del Valle. 2001. Ecological lessons and applications from one century of low external-input farming in the pampas of Argentina. Agriculture, Ecosystems and Environment 83(1-2):65-81. https://doi.org/10.1016/S0167-8809(00)00155-9.

Wang, H., R. Zhu, X. Zhang, Y. Li, L. Ni, P. Xie, and H. Shen. 2019. Abiotic environmental factors override phytoplankton succession in shaping both free-living and attached bacterial communities in a highland lake. AMB Express 9:170. https://doi.org/10.1186/s13568-019-0889-z.

Wei, C., S. Bao, X. Zhu, and X. Huang. 2008. Spatio-temporal variations of the bacterioplankton community composition in Chaohu Lake, China. Progress in Natural Science 18(9):1115-1122. https://doi.org/10.1016/j.pnsc.2008.04.005.

Whitman, W. B., D. C., Coleman, and W. J. Wiebe. 1998. Prokaryotes: The unseen majority. Proc Natl Acad Sci USA 95:6578-6583.

Wu, X., W. Xi, W. Ye, and H. Yang. 2007. Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiology Ecology 61(1):85-96. https://doi.org/10.1111/j.1574-6941.2007.00326.x.

Yilmaz, P., L. W. Parfrey, P. Yarza, J. Gerken, E. Pruesse, C. Quast, T. Schweer, J. Peplies, W. Ludwig, and F. O. Glöckner. 2014. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acid Research. 42:D643-D648. https://doi.org/10.1093/nar/gkt1209.

Zaila, K. E., T. G. Doak, H. Ellerbrock, C. H. Tung, M. L. Martins, D. Kolbin, M.-C. Yao, D. M. Cassidy-Hanley, T. G. Clark, and W.-J. Chang. 2017. Diversity and Universality of Endosymbiotic Rickettsia in the Fish Parasite Ichthyophthirius multifiliis. Frontiers in Microbiology 8:189. https://doi.org/10.3389/fmicb.2017.00189.

Zhao, M., Y. T. Ma, S. Y. He, X. Mou, and L. Wu. 2020. Dynamics of bacterioplankton community structure in response to seasonal hydrological disturbances in Poyang Lake, the largest wetland in China. FEMS Microbiol Ecol 96(8):fiaa064. https://doi.org/10.1093/femsec/fiaa064.

Zhou, L., W. Chen, J. Sun, L. Liu, and X. Huang. 2020. Spatial Variation in Bacterioplankton Communities in the Pearl River, South China: Impacts of Land Use and Physicochemical Factors. Microorganisms 8(6):814. https://doi.org/10.3390/microorganisms80608.

Estructura y dinámica del bacterioplancton en cuatro lagunas pampeanas de la cuenca del río Salado (Buenos Aires, Argentina)

Published

2022-05-25 — Updated on 2022-11-15

Versions

How to Cite

Nuozzi, G., Seoane Rocha, C., Sagua, M., Llames, M. E., Huber, P., Metz, S., Lagomarsino, L., & Schiaffino, M. R. (2022). Structure and dynamics of bacterioplankton from four Pampean shallow lakes of the Salado River basin (Buenos Aires, Argentina). Ecología Austral, 32(2), 343–360. https://doi.org/10.25260/EA.22.32.2.0.1811 (Original work published May 25, 2022)