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Productivity and rainfall drive bacterial metabolism in tropical cascading reservoirs

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Abstract

Tropical reservoirs are main carbon sources to the atmosphere, and bacterial metabolism is a key process in these emissions. Here, we explored the drivers of bacterial metabolism in four tropical cascading reservoirs forming a trophic state gradient, and compared them with those found in the literature (mainly from temperate regions). Bacterial production (BP) and growth efficiency (BGE) responded to trophic state-related variables, while bacterial respiration (BR) was weakly and negatively correlated to dissolved organic carbon (DOC). BP and BGE were higher in reservoirs with higher primary production, while BR (high throughout the whole study period) was greater in less productive reservoirs, where planktonic communities were often limited by phosphorus. The high BR and low BGE observed in less productive downstream reservoirs (i.e., less nutrients and organic matter availability) may be explained by increasing nutrient limitation and proportion of recalcitrant DOC along the cascade. Despite the lower productivity, oligotrophic reservoirs may be more important in terms of carbon biogeochemistry, considering that microbes in those systems mineralize more carbon than upstream productive reservoirs. Moreover, the drivers of bacterial metabolism may act differently according to latitude, as seasonality in the tropics is determined mainly by rainfall rather than temperature.

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References

  • Adams, H. E., B. C. Crump & G. W. Kling, 2010. Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environmental microbiology 12: 1319–1333.

    Article  CAS  PubMed  Google Scholar 

  • Amado, A. M., F. Meirelles-Pereira, L. O. Vidal, H. Sarmento, A. L. Suhett, V. F. Farjalla, J. B. Cotner & F. Roland, 2013. Tropical freshwater ecosystems have lower bacterial growth efficiency than temperate ones. Frontiers in Microbiology 4: 167.

    Article  PubMed  PubMed Central  Google Scholar 

  • ANA, 2016. Agência Nacional das Águas.

  • Apple, J. K., P. A. del Giorgio & W. M. Kemp, 2006. Temperature regulation of bacterial production, respiration, and growth efficiency in a temperate salt-marsh estuary. Aquatic Microbial Ecology 43: 243–254.

    Article  Google Scholar 

  • Barbosa, F. A. R., J. Padisák, E. L. G. Espindola, G. Borics & O. Rocha, 1999. The cascading reservoir continuum concept (CRCC) and its application to the river Tietê-basin, São Paulo State, Brazil. Theoretical Reservoir Ecology and its Applications 1: 425–437.

    Google Scholar 

  • Barros, N., J. J. Cole, L. J. Tranvik, Y. T. Prairie, D. Bastviken, V. L. M. Huszar, P. del Giorgio & F. Roland, 2011. Carbon emission from hydroelectric reservoirs linked to reservoir age and latitude. Nature Geoscience 4: 593–596.

    Article  CAS  Google Scholar 

  • Berggren, M., H. Laudon & M. Jansson, 2009. Aging of allochthonous organic carbon regulates bacterial production in unproductive boreal lakes. Limnology and Oceanography 54: 1333–1342.

    Article  CAS  Google Scholar 

  • Berggren, M., H. Laudon, A. Jonsson & M. Jansson, 2010. Nutrient Constraints on Metabolism Affect the Temperature Regulation of Aquatic Bacterial Growth Efficiency. Microbial Ecology 60: 894–902.

    Article  CAS  PubMed  Google Scholar 

  • Bergstrom, A. & M. Jansson, 2000. Bacterioplankton Production in Humic Lake Ortrasket in Relation to Input of Bacterial Cells and Input of Allochthonous Organic Carbon. Microbial Ecology 39: 101–115.

    Article  CAS  PubMed  Google Scholar 

  • Berman, T., Y. Z. Yacobi, A. Parparov & G. Gal, 2010. Estimation of long-term bacterial respiration and growth efficiency in Lake Kinneret. FEMS microbiology ecology 71: 351–363.

    Article  CAS  PubMed  Google Scholar 

  • Bertilsson, S., A. Eiler, A. Nordqvist & N. O. Jorgensen, 2007. Links between bacterial production, amino-acid utilization and community composition in productive lakes. The ISME journal 1: 532–544.

    Article  CAS  PubMed  Google Scholar 

  • Biddanda, B., M. Ogdahl & J. Cotner, 2001. Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnology and Oceanography 46: 730–739.

    Article  Google Scholar 

  • Biddanda, B., 2017. Global Significance of the Changing Freshwater Carbon Cycle. Eos.

  • Borsheim, K. Y. & S. M. Myklestad, 1997. Dynamics of DOC in the Norwegian Sea inferred from monthly profiles collected during 3 years at 66 degrees N, 2 degrees E. Deep-Sea Research Part I-Oceanographic Research Papers 44: 593–601.

    Article  Google Scholar 

  • Briand, E., O. Pringault, S. Jacquet & J. P. Torréton, 2004. The use of oxygen microprobes to measure bacterial respiration for determining bacterioplankton growth efficiency. Limnology and Oceanography: Methods 2: 406–416.

    Article  Google Scholar 

  • Cammack, W. L., J. Kalff, Y. T. Prairie & E. M. Smith, 2004. Fluorescent dissolved organic matter in lakes: relationships with heterotrophic metabolism. Limnology and Oceanography 49: 2034–2045.

    Article  Google Scholar 

  • Carlson, C., P. del Giorgio & G. Herndl, 2007. Microbes and the Dissipation of Energy and Respiration: from Cells to Ecosystems. Oceanography 20: 89–100.

    Article  Google Scholar 

  • Chróst, R., M. Koton & W. Siuda, 2000. Bacterial secondary production and bacterial biomass in four Mazurian lakes of differing trophic status. Polish Journal of Environmental Studies 9: 255–266.

    Google Scholar 

  • Chrzanowski, T. H. & J. G. Hubbard, 1988. Primary and bacterial secondary production in a southwestern reservoir. Applied and environmental microbiology 54: 661–669.

    PubMed  PubMed Central  Google Scholar 

  • Cimbleris, A. C. & J. Kalff, 1998. Planktonic bacterial respiration as a function of C: N: P ratios across temperate lakes. Hydrobiologia 384: 89–100.

    Article  Google Scholar 

  • Cole, J. J., N. F. Caraco, G. W. Kling & T. K. Kratz, 1994. Carbon dioxide supersaturation in the surface waters of lakes. Science 265: 1568–1569.

    Article  CAS  PubMed  Google Scholar 

  • Cole, J. J., Y. T. Prairie, N. F. Caraco, W. H. McDowell, L. J. Tranvik, R. G. Striegl, C. M. Duarte, P. Kortelainen, J. A. Downing, J. J. Middelburg & J. Melack, 2007. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10: 172–185.

    Article  Google Scholar 

  • Cotner, J. B. & B. A. Biddanda, 2002. Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5: 105–121.

    Article  CAS  Google Scholar 

  • Cunha-Santino, M. B., Â. T. Fushita & I. Bianchini, 2017. A modeling approach for a cascade of reservoirs in the Juquiá-Guaçu River (Atlantic Forest, Brazil). Ecological Modelling 356: 48–58.

    Article  Google Scholar 

  • del Giorgio, P. A. & J. J. Cole, 1998. Bacterial growth efficiency in natural aquatic systems. Annual Review of Ecology and Systematics 29: 503–541.

    Article  Google Scholar 

  • Descy, J.-P., B. Leporcq, L. Viroux, C. François & P. Servais, 2002. Phytoplankton production, exudation and bacterial reassimilation in the River Meuse (Belgium). Journal of Plankton Research 24: 161–166.

    Article  Google Scholar 

  • Domingues, C. D., L. H. da Silva, L. M. Rangel, L. de Magalhaes, A. de Melo Rocha, L. M. Lobao, R. Paiva, F. Roland & H. Sarmento, 2016. Microbial Food-Web Drivers in Tropical Reservoirs. Microbial Ecology 73: 505–520.

    Article  PubMed  Google Scholar 

  • DuBois, M., K. A. Gilles, J. K. Hamilton, P. T. Rebers & F. Smith, 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28: 350–356.

    Article  CAS  Google Scholar 

  • Fearnside, P. M., 2005. Do hydroelectric dams mitigate global warming? The case of Brazil’s Curuá-Una Dam. Mitigation and Adaptation Strategies for Global Change 10: 675–691.

    Article  Google Scholar 

  • Fouilland, E. & B. Mostajir, 2010. Revisited phytoplanktonic carbon dependency of heterotrophic bacteria in freshwaters, transitional, coastal and oceanic waters. FEMS Microbial Ecology 73: 419–429.

    Article  CAS  Google Scholar 

  • Gasol, J. M. & P. A. del Giorgio, 2000. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Scientia Marina 64: 197–224.

    Article  Google Scholar 

  • Guenet, B., M. Danger, L. Harrault, B. Allard, M. Jauset-Alcala, G. Bardoux, D. Benest, L. Abbadie & G. Lacroix, 2013. Fast mineralization of land-born C in inland waters: first experimental evidences of aquatic priming effect. Hydrobiologia 721: 35–44.

    Article  Google Scholar 

  • Guillemette, F., S. Leigh McCallister & P. A. del Giorgio, 2016. Selective consumption and metabolic allocation of terrestrial and algal carbon determine allochthony in lake bacteria. ISME J 10: 1373–1382.

    Article  CAS  PubMed  Google Scholar 

  • Healey, F. P. & L. L. Hendzel, 1979. Indicators of Phosphorus and Nitrogen Deficiency in Five Algae in Culture. Journal of the Fisheries Research Board of Canada 36: 1364–1369.

    Article  CAS  Google Scholar 

  • Hotchkiss, E., R. Hall, M. Baker, E. Rosi-Marshall & J. Tank, 2014. Modeling priming effects on microbial consumption of dissolved organic carbon in rivers. Journal of Geophysical Research: Biogeosciences 119: 982–995.

    CAS  Google Scholar 

  • INMET, 2016. Instituto nacional de Meteorologia.

  • Jansson, M., T. Hickler, A. Jonsson & J. Karlsson, 2008. Links between Terrestrial Primary Production and Bacterial Production and Respiration in Lakes in a Climate Gradient in Subarctic Sweden. Ecosystems 11: 367–376.

    Article  CAS  Google Scholar 

  • Jugnia, L.-B., T. Sime-Ngando & J. Devaux, 2006. Relationship between bacterial and primary production in a newly filled reservoir: temporal variability over 2 consecutive years. Ecological Research 22: 321–330.

    Article  Google Scholar 

  • Kamjunke, N., M. R. Oosterwoud, P. Herzsprung & J. Tittel, 2016. Bacterial production and their role in the removal of dissolved organic matter from tributaries of drinking water reservoirs. The Science of the Total Environment 548–549: 51–59.

    Article  PubMed  Google Scholar 

  • Kilham, P. & S. S. Kilham, 1990. Endless summer: internal loading processes dominate nutrient cycling in tropical lakes. Freshwater Biology 23: 379–389.

    Article  Google Scholar 

  • Kirchman, D., E. K’nees & R. Hodson, 1985. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Applied and Environmental Microbiology 49: 599–607.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kritzberg, E. S., J. J. Cole, M. M. Pace & W. Granéli, 2005. Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquatic Microbial Ecology 38: 103–111.

    Article  Google Scholar 

  • Lewis Jr., W. M., 1987. Tropical limnology. Annual Review of Ecology and Systematics 18: 159–184.

    Article  Google Scholar 

  • Lewis, W. M., 1996. Tropical lakes: how latitude makes a difference. Perspectives in tropical limnology, 43–64.

  • Lorenzen, C. J., 1967. Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnology and oceanography 12: 343–346.

    Article  CAS  Google Scholar 

  • Mackereth, F. J. H., J. Heron & J. F. Talling, 1978. Water analys is: some revised methods for limnologists. Freshwater Biological Association.

  • Marker, A., 1980. The measurement of photosynthetic pigments in freshwaters and standardization of methods: conclusions and recommendations. Archiv für Hydrobiologie–BeiheftErgebnisse der Limnologie 14:91-106.

  • Marotta, H., L. Pinho, C. Gudasz, D. Bastviken, L. J. Tranvik & A. Enrich-Prast, 2014. Greenhouse gas production in low-latitude lake sediments responds strongly to warming. Nature Climate Change 4: 467–470.

    Article  CAS  Google Scholar 

  • Meyer, J. L., 1994. The microbial loop in flowing waters. Microbial Ecology 28: 195–199.

    Article  CAS  PubMed  Google Scholar 

  • Morana, C., H. Sarmento, J.-P. Descy, J. M. Gasol, A. V. Borges, S. Bouillon & F. Darchambeau, 2014. Production of dissolved organic matter by phytoplankton and its uptake by heterotrophic prokaryotes in large tropical lakes. Limnology and Oceanography 59: 1364–1375.

    Article  CAS  Google Scholar 

  • Mush, E., 1980. Comparison of different methods for chlorophyll and phaeopigment determination. Archiv für Hydrobiologie–BeiheftErgebnisse der Limnologie 14:14-36.

  • R Core Team, 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing.

  • Ram, A. P., D. Boucher, T. Sime-Ngando, D. Debroas & J. C. Romagoux, 2005. Phage bacteriolysis, protistan bacterivory potential, and bacterial production in a freshwater reservoir: coupling with temperature. Microbial Ecology 50: 64–72.

    Article  Google Scholar 

  • Ram, A. S., S. Palesse, J. Colombet, M. Sabart, F. Perriere & T. Sime-Ngando, 2013. Variable viral and grazer control of prokaryotic growth efficiency in temperate freshwater lakes (French Massif Central). Microbial Ecology 66: 906–916.

    Article  CAS  PubMed  Google Scholar 

  • Ram, A. P., J. Colombet, F. Perriere, A. Thouvenot & T. Sime-Ngando, 2015. Viral and grazer regulation of prokaryotic growth efficiency in temperate freshwater pelagic environments. FEMS Microbiology Ecology 91: 1–12.

    Google Scholar 

  • Ram, A. S. P., J. Colombet, F. Perriere, A. Thouvenot & T. Sime-Ngando, 2016. Viral Regulation of Prokaryotic Carbon Metabolism in a Hypereutrophic Freshwater Reservoir Ecosystem (Villerest, France). Frontiers in Microbiology 7.

  • Raymond, P. A., J. Hartmann, R. Lauerwald, S. Sobek, C. McDonald, M. Hoover, D. Butman, R. Striegl, E. Mayorga & C. Humborg, 2013. Global carbon dioxide emissions from inland waters. Nature 503: 355–359.

    Article  CAS  PubMed  Google Scholar 

  • Robarts, R. D. & R. J. Wicks, 1990. Heterotrophic bacterial production and its dependence on autotrophic production in a hypertrophic African reservoir. Canadian Journal of Fisheries and Aquatic Sciences 47: 1027–1037.

    Article  Google Scholar 

  • Robarts, R. D., M. T. Arts, M. S. Evans & M. J. Waiser, 1994. The coupling of heterotrophic bacterial and phytoplank ton production in a hypertrophic, shallow prairie lake. Canadian Journal of Fisheries and Aquatic Sciences 51: 2219–2226.

    Article  Google Scholar 

  • Roiha, T., S. Peura, M. Cusson & M. Rautio, 2016. Allochthonous carbon is a major regulator to bacterial growth and community composition in subarctic freshwaters. Scientific Reports 6: 34456.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarmento, H., F. Unrein, M. Isumbisho, S. Stenuite, J. M. Gasol & J. P. Descy, 2008. Abundance and distribution of picoplankton in tropical, oligotrophic Lake Kivu, eastern Africa. Freshwater Biology 53: 756–771.

    Article  Google Scholar 

  • Sarmento, H., 2012. New paradigms in tropical limnology: the importance of the microbial food web. Hydrobiologia 686: 1–14.

    Article  Google Scholar 

  • Sarmento, H., E. O. Casamayor, J. C. Auguet, M. Vila-Costa, M. Felip, L. Camarero & J. M. Gasol, 2015. Microbial food web components, bulk metabolism, and single-cell physiology of piconeuston in surface microlayers of high-altitude lakes. Frontiers in Microbiology 6: 361.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarmento, H., C. Morana & J. M. Gasol, 2016. Bacterioplankton niche partitioning in the use of phytoplankton-derived dissolved organic carbon: quantity is more important than quality. The ISME journal 10: 2582–2592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scofield, V., S. M. Jacques, J. R. Guimaraes & V. F. Farjalla, 2015. Potential changes in bacterial metabolism associated with increased water temperature and nutrient inputs in tropical humic lagoons. Frontiers in Microbiology 6: 310.

    Article  PubMed  PubMed Central  Google Scholar 

  • Simon, M. & F. Azam, 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Marine ecology progress series Oldendorf 51: 201–213.

    Article  CAS  Google Scholar 

  • Simon, M. & M. M. Tilzer, 1987. Bacterial response to seasonal changes in primary production and phytoplankton biomass in Lake Constance. Journal of Plankton Research 9: 535–552.

    Article  Google Scholar 

  • Simon, M., B. C. Cho & F. Azam, 1992. Significance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications. Marine Ecology Progress Series 86: 103–110.

    Article  Google Scholar 

  • Smith, E. M. & Y. T. Prairie, 2004. Bacterial metabolism and growth efficiency in lakes: the importance of phosphorus availability. Limnology and Oceanography 49: 137–147.

    Article  CAS  Google Scholar 

  • Straskraba, M., 1990. Limnological particularities of multiple reservoir series. Archiv fur Hydrobiologie Beiheft Ergebnisse der Limnologie 33: 677–678.

    Google Scholar 

  • Tranvik, L. J., J. A. Downing, J. B. Cotner, S. A. Loiselle, R. G. Striegl, T. J. Ballatore, P. Dillon, K. Finlay, K. Fortino & L. B. Knoll, 2009. Lakes and reservoirs as regulators of carbon cycling and climate. Limnology and Oceanography 54: 2298–2314.

    Article  CAS  Google Scholar 

  • Tulonen, T., 1993. Bacterial production in a mesohumic lake estimated from [14C] leucine incorporation rate. Microbial Ecology 26: 201–217.

    Article  CAS  PubMed  Google Scholar 

  • Vidal, L. O., G. Abril, L. F. Artigas, L. M. Melo, M. C. Bernardes, L. M. Lobão, M. C. Reis, P. Moreira-Turcq, M. Benedetti, V. L. Tornisielo & F. Roland, 2015. Hydrological pulse regulating the bacterial heterotrophic metabolism between Amazonian mainstems and floodplain lakes. Frontiers in Microbiology 6: 1054.

    Article  PubMed  PubMed Central  Google Scholar 

  • White, P. A., J. Kalff, J. B. Rasmussen & J. M. Gasol, 1991. The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats. Microbial Ecology 21: 99–118.

    Article  CAS  PubMed  Google Scholar 

  • WMO, 2016. The Climate Global in 2011-2015. World Meteorological Organization.

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Acknowledgements

This research was funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP processes 2014/14139-3 and 2011/50054-4). We are thankful to the Editor of Hydrobiologia, two anonymous reviewers, André Megali Amado and Odete Rocha for valuable comments that helped to improve our manuscript.

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  1. Department of Hydrobiology (DHb), Laboratory of Microbial Processes and Biodiversity, Universidade Federal de São Carlos (UFSCar), São Carlos, SP, Brazil

    Roberta Freitas, Michaela Ladeira de Melo & Hugo Sarmento

  2. Department of Botany (DB), Laboratory of Phycology, Universidade Federal de São Carlos (UFSCar), São Carlos, SP, Brazil

    Helena Henriques Vieira, Guilherme Pavan de Moraes & Armando Augusto Henriques Vieira

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  1. Roberta Freitas
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  2. Helena Henriques Vieira
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Freitas, R., Vieira, H.H., de Moraes, G.P. et al. Productivity and rainfall drive bacterial metabolism in tropical cascading reservoirs. Hydrobiologia 809, 233–246 (2018). https://doi.org/10.1007/s10750-017-3472-0

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