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Bacterial production, abundance and cell properties in boreal estuaries: relation to dissolved organic matter quantity and quality

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Abstract

Estuarine bacteria are key modifiers of allochthonous matter entering the sea, and thereby control major biogeochemical processes such as nutrient cycling and organic matter transformation. In a highly dynamic estuarine environment, bacterial growth and activity are regulated by multiple factors including the availability of organic carbon, inorganic nutrient concentrations, salinity and temperature. The variability of estuarine bacterial communities in relation to environmental factors and dissolved organic matter (DOM) quantity and quality was studied in three Baltic Sea estuaries with different catchment characteristics, flow and mixing regimes. The work was conducted during six consecutive seasons over 2 years. Bacterial activity, biomass and cytometric cell population characteristics were studied against an suite of environmental parameters and DOM quality and quantity (Salinity, DOC, DON and DIN concentration, SUVA254, UV Slope275–295, Fluoresecence peaks A and T, and Apparent mean molecular weight). Environmental variables and DOM quality varied significantly between rivers, indicating influence of catchment characteristics. Bacterial biomass varied significantly between the sampling seasons, and bacterial production also varied between the rivers, indicating an influence of DOM quality on bacterial activity. Based on cytometric grouping into low- and high- nucleic acid bacterial populations (LNA and HNA, respectively) salinity-dependent and salinity-independent clusters of bacterial variables were identified. The results suggest that the LNA clusters were not directly dependent on salinity, but possibly linked to humic substance degradation, whereas the HNA clusters were linked to salinity-correlated environmental variables reflecting DOM quality. Mixed-effects regression modeling of bacterial biomass turnover time suggests DOM fluorescence properties to be useful proxies of bioavailability. Our study shows that growth and community dynamics of estuarine bacteria may be partially regulated by quality of riverine DOM, and cytometric sub-populations of estuarine bacteria have differing regulative factors.

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References

  • Alling V, Humborg C, Mörth CM, Rahm L, Pollehne F (2008) Tracing terrestrial organic matter by δ34S and δ13C signatures in a subarctic estuary. Limnology and Oceanography 53(6):2594–2602.

    Article  CAS  Google Scholar 

  • Andersson AF, Riemann L, Bertilsson S (2009) Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J 4:171–181

    Article  PubMed  Google Scholar 

  • Apple JK, Smith EM, Boyd TJ (2008) Temperature, salinity, nutrients, and the covariation of bacterial production and chlorophyll-a in estuarine ecosystems. J Coast Res 10055:59–75

    Article  Google Scholar 

  • Asmala E, Autio R, Kaartokallio H, Pitkänen L, Stedmon C, Thomas DN (2013) Bioavailability of riverine dissolved organic matter in three Baltic Sea estuaries and the effect of catchment land use. Biogeosciences 10:6969–6986

    Article  CAS  Google Scholar 

  • Asmala E, Bowers DG, Autio R, Kaartokallio H, Thomas DN (2014a) Qualitative changes of riverine dissolved organic matter at low salinities due to flocculation. J Geophys Res Biogeosci 119:1919–1933

    Article  CAS  Google Scholar 

  • Asmala E, Autio R, Kaartokallio H, Stedmon CA, Thomas DN (2014b). Processing of humic-rich riverine dissolved organic matter by estuarine bacteria: effects of predegradation and inorganic nutrients. Aquat Sci 76:451–463

    Article  CAS  Google Scholar 

  • Autio R (1998) Response of seasonally cold-water bacterioplankton to temperature and substrate treatments. Est Coast Shelf Sci 46:465–474

    Article  Google Scholar 

  • Barton K (2015). MuMIn: Multi-Model Inference. R package version 1.14.0. http://CRAN.R-project.org/package=MuMIn

  • Bates D, Maechler M, Bolker BM and Walker S (2014) “lme4: Linear mixed-effects models using Eigen and S4.” ArXiv e-print; submitted to _Journal of Statistical Software. http://www.arxiv.org/abs/1406.5823. Accessed 14 May 2015

  • Bauer JE, Bianchi TS (2011) Dissolved organic carbon cycling and transformation. Treat est coast sci 5:7–67

    Article  Google Scholar 

  • Blum LK, Mills AL (2012) Estuarine Microbial Ecology, in Estuarine Ecology, Second Edition (eds JW Day, BC Crump, WM Kemp, A Yáñez-Arancibia), John Wiley & Sons, Inc., Hoboken, NJ, USA. doi: 10.1002/9781118412787.ch9

  • Bouvier TC, del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453–470

    Article  CAS  Google Scholar 

  • Bouvier T, Del Giorgio PA, Gasol JM (2007) A comparative study of the cytometric characteristics of High and Low nucleic-acid bacterioplankton cells from different aquatic ecosystems. Environ Microbiol 9:2050–2066

    Article  CAS  PubMed  Google Scholar 

  • Boyd TJ, Osborn CL (2004) Changes in CDOM fluorescence from allochthonous and autochthonous sources during tidal mixing and bacterial degradation in two coastal estuaries. Mar Chem 89:189–210

    Article  CAS  Google Scholar 

  • Cauwet G, Déliat G, Krastev A, Shtereva G, Becquevort S, Lancelot C, Popa L (2002) Seasonal DOC accumulation in the Black Sea: a regional explanation for a general mechanism. Mar Chem 79:193–205

    Article  CAS  Google Scholar 

  • Coble PG (1996) Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Mar Chem 51:325–346

    Article  CAS  Google Scholar 

  • Cottrell MT, Kirchman DL (2004) Single-cell analysis of bacterial growth, cell size, and community structure in the Delaware estuary. Aquat Microb Ecol 34:139–149

    Article  Google Scholar 

  • Deutsch B, Alling V, Humborg C, Korth F, Mörth CM (2012) Tracing inputs of terrestrial high molecular weight dissolved organic matter within the Baltic Sea ecosystem. Biogeosciences 9(11):4465–4475.

    Article  CAS  Google Scholar 

  • Findlay S, Sinsabaugh RL (Eds) (2003) Aquatic ecosystems: Interactivity of dissolved organic matter. Academic Press, Boston

  • Fleming-Lehtinen V, Räike A, Kortelainen P, Kauppila P, Thomas DN (2014) Organic Carbon Concentration in the Northern Coastal Baltic Sea between 1975 and 2011. Estuaries Coast 38:466–481

    Article  Google Scholar 

  • Fortunato CS, Herfort L, Zuber P, Baptista AM, Crump BC (2011) Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient. ISME J 6:554–563

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuhrman JA, Azam F (1980) Bacterioplankton secondary production estimates for coastal waters of British Columbia Antarctica and California. Appl Environ Microbiol 39:1085–1095  

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fukuda R, Ogawa H, Nagata T, Koike I (1998) Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl environ microbiol 64(9):3352–3358

    Google Scholar 

  • Gasol JM, Del Giorgio PA (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci Mar. 64:197–224

    Article  Google Scholar 

  • Gasol JM, Zweifel UL, Peters F, Fuhrman JA, Hagström Å (1999) Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Appl Environ Microbiol 65:4475–4483

    CAS  PubMed  PubMed Central  Google Scholar 

  • del Giorgio PA, Bouvier TC (2002). Linking the physiologic and phylogenetic successions in free‐living bacterial communities along an estuarine salinity gradient. Limnol Oceanogr 47(2);471-486.

  • Granskog M, Kaartokallio H, Kuosa H, Thomas DN, Vainio J (2006) Sea ice in the Baltic Sea–a review. Est Coast Shelf Sci 70:145–160

    Article  Google Scholar 

  • Grasshoff K, Ehrhardt MKK (1983) Methods of Seawater Analysis. Verlag Chemie GmbH, Weinheim

    Google Scholar 

  • Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoikkala L, Aarnos H, Lignell R (2009) Changes in nutrient and carbon availability and temperature as factors controlling bacterial growth in the northern Baltic Sea. Estuaries and coasts 32(4):720–733.

  • Hoikkala L, Kortelainen P, Soinne H, Kuosa H (2015) Dissolved organic matter in the Baltic Sea. Journal of Marine Systems 142:47–61

  • Hopkinson CS, Buffam I, Hobbie J, Vallino J, Perdue M, Eversmeyer B, Foreman K (1998) Terrestrial inputs of organic matter to coastal ecosystems: an intercomparison of chemical characteristics and bioavailability. Biogeochemistry 43:211–234

    Article  CAS  Google Scholar 

  • Hulatt CJ, Kaartokallio H, Asmala E, Autio R, Stedmon CA, Sonninen E, Thomas DN (2014a) Bioavailability and radiocarbon age of fluvial dissolved organic matter (DOM) from a northern peatland-dominated catchment: effect of land-use change. Aquat Sci 76:393–404

  • Hulatt CJ, Kaartokallio H, Oinonen M, Sonninen E, Stedmon CA, Thomas DN (2014b) Radiocarbon dating of fluvial organic matter reveals land-use impacts in Boreal Peatlands. Env Sci Tech 48:12543–12551

    Article  CAS  Google Scholar 

  • Jickells TD (1998) Nutrient biogeochemistry of the coastal zone Science 281:217–222

    CAS  PubMed  Google Scholar 

  • Johnes P, Moss B, Phillips G (1996) The determination of total nitrogen and total phosphorus concentrations in freshwaters from land use stock headage and population data: testing of a model for use in conservation and water quality management. Freshw Biol 36:451–473

    Article  CAS  Google Scholar 

  • Kalbitz K, Schmerwitz J, Schwesig D, Matzner E (2003) Biodegradation of soil-derived dissolved organic matter as related to its properties. Geoderma 113:273–291

    Article  CAS  Google Scholar 

  • Kirchman DL (2010) Microbial ecology of the oceans., Vol 36John Wiley & Sons, New York

    Google Scholar 

  • Kirchman DL, Keil RG, Wheeler PA (1989). The effect of amino acids on ammonium utilization and regeneration by heterotrophic bacteria in the subarctic Pacific. Deep Sea Res A 36(11):1763–1776

  • Kirchman D, K’nees E, Hodson R (1985) Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49:599–607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kirchman DL, Dittel AI, Findlay SE, Fischer D (2004) Changes in bacterial activity and community structure in response to dissolved organic matter in the Hudson River New York. Aquat Microb Ecol 35:243–257

    Article  Google Scholar 

  • Kisand V, Rocker D, Simon M (2008) Significant decomposition of riverine humic-rich DOC by marine but not estuarine bacteria assessed in sequential chemostat experiments. Aquat Microb Ecol 53:151–160

    Article  Google Scholar 

  • Kortelainen P, Saukkonen S, Mattsson T (1997) Leaching of nitrogen from forested catchments in Finland. Glob Biogeochem Cycles 11:627–638

    Article  CAS  Google Scholar 

  • Langenheder S, Kisand V, Wikner J, Tranvik LJ (2003) Salinity as a structuring factor for the composition and performance of bacterioplankton degrading riverine DOC. FEMS microbiol ecol 45(2):189–202

  • Lauro FM, McDougald D, Thomas T, Williams TJ, Egan S, Rice S, DeMaere MZ, Ting L, Ertan H, Johnson J, Ferriera S, Lapidus A, Anderson I, Kyrpides N, Munk ACm Dteer C, Han CS, Brown MV, Robb, FT, Kjelleberg S, Cavicchioli R (2009) The genomic basis of trophic strategy in marine bacteria. Proc Nat Acad Sci 106(37):15527–15533

  • Longnecker K, Sherr BF, Sherr EB (2005) Activity and phylogenetic diversity of bacterial cells with high and low nucleic acid content and electron transport system activity in an upwelling ecosystem. Appl Environ Microbiol 71:7737–7749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malcolm R (1990) The uniqueness of humic substances in each of soil stream and marine environments. Anal Chim Acta 232:19–30

    Article  CAS  Google Scholar 

  • Mary I, Heywood JL, Fuchs BM, Amann R, Tarran GA, Burkill PH, Zubkov MV (2006) SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect. Aquat Microb Ecol 45:107–113

    Article  Google Scholar 

  • Mattsson T, Kortelainen P, Räike A, Lepistö A, Thomas DN (2015) Spatial and temporal variability of organic C and N concentrations and export from 30 boreal rivers induced by land use and climate. Sci Tot Environ 508:145–154

  • McKenna JH (2004) DOC dynamics in a small temperate estuary: simultaneous addition and removal processes and implications on observed nonconservative behavior. Estuaries 27:604–616

    Article  CAS  Google Scholar 

  • Moran MA, Hodson RE (1990) Bacterial production on humic and nonhumic components of dissolved organic carbon. Limnol Oceanogr 35:1744–1756

    Article  CAS  Google Scholar 

  • Murphy KR, Butler KD, Spencer RG, Stedmon CA, Boehme JR, Aiken GR (2010) Measurement of dissolved organic matter fluorescence in aquatic environments: an interlaboratory comparison. Env Sci Tech 44:9405–9412

    Article  CAS  Google Scholar 

  • Norman L, Thomas DN (2014) Long-term storage of riverine dissolved organic carbon. Technical note, ResearchGate. doi:10.13140/2.1.3331.5200

    Google Scholar 

  • Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens HH, Wagner H (2015) vegan: Community Ecology Package. R package version 2.3-1. http://CRAN.R-project.org/package=vegan

  • Opsahl S, Benner R (1997) Distribution and cycling of terrigenous dissolved organic matter in the ocean. Nature 386:480–482

    Article  CAS  Google Scholar 

  • Pinhassi J, Hagström Å (2000) Seasonal succesion in marine bacterioplankton Aquat Microb Ecol. 21:245–256

    Article  Google Scholar 

  • Pinhassi J, Gómez-Consarnau L, Alonso-Sáez L, Sala MM, Vidal M, Pedrós-Alió C, Gasol JM (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44:241

    Article  Google Scholar 

  • Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23:187–204

    Article  Google Scholar 

  • Qian J, Mopper K (1996) Automated high-performance high-temperature combustion total organic carbon analyzer. Anal Chem 68:3090–3097

    Article  CAS  Google Scholar 

  • Raymond PA, Spencer RGM (2014) Riverine DOM. In: Hansell DA, Carlson CA (Eds.) Biogeochemistry of Marine Dissolved Organic Matter. 2nd edn. Academic Press, Boston

  • Revelle W (2013) Psych package: procedures for personality and psychological research. Northwestern University, Evanston

    Google Scholar 

  • Riemann B, Bjørnsen PK, Newell S, Fallon R (1987) Calculation of cell production of coastal marine bacteria based on measured incorporation of [3H] thymidine. Limnol Oceanogr 32(2):471–476

  • Riemann L, Steward GF, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocker D, Kisand V, Scholz-Böttcher B, Kneib T, Lemke A, Rullkötter J, Simon M (2012) Differential decomposition of humic acids by marine and estuarine bacterial communities at varying salinities. Biogeochemistry 111:331–346

    Article  CAS  Google Scholar 

  • Sachse A, Henrion R, Gelbrecht J, Steinberg CEW (2005) Classification of dissolved organic carbon (DOC) in river systems: influence of catchment characteristics and autochthonous processes. Org Geochem 36:923–935  

    Article  CAS  Google Scholar 

  • Simon M, Azam F (1989). Protein content and protein synthesis rates of planktonic marine bacteria. Mar ecol prog ser 51(3):201–213

  • Stedmon CA, Markager S, Kaas H (2000) Optical properties and signatures of chromophoric dissolved organic matter (CDOM) in Danish coastal waters. Est Coast Shelf Sci 51:267–278

    Article  CAS  Google Scholar 

  • Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    Article  CAS  PubMed  Google Scholar 

  • Talarmin A, Van Wambeke F, Catala P, Courties C, Lebaron P (2011) Flow cytometric assessment of specific leucine incorporation in the open Mediterranean. Biogeosciences 8:253–265

    Article  CAS  Google Scholar 

  • Troussellier M, Schafer H, Batailler N, Bernard L, Courties C, Lebaron P, Vives-Rego J (2002) Bacterial activity and genetic richness along an estuarine gradient (Rhone River plume France). Aquat Microb Ecol 28:13–24

    Article  Google Scholar 

  • Vartiainen T, Liimatainen A, Kauranen P (1987) The use of TSK size exclusion columns in determination of the quality and quantity of humus in raw waters and drinking waters. Sci Tot Environ 62:75–84

    Article  CAS  Google Scholar 

  • Wang Y, Hammes F, Boon N, Chami M, Egli T (2009) Isolation and characterization of low nucleic acid (LNA)-content bacteria. ISME J 3:889–902

    Article  CAS  PubMed  Google Scholar 

  • Weishaar JL, Aiken GR, Bergamaschi BA, Fram MS, Fujii R, Mopper K (2003) Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Env Sci Techn 37:4702–4708

    Article  CAS  Google Scholar 

  • Wikner J, Cuadros R, Jansson M (1999) Differences in consumption of allochthonous DOC under limnic and estuarine conditions in a watershed. Aquat Microb Ecol 17:289–299

    Article  Google Scholar 

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Acknowledgments

This study was supported by grants from the Academy of Finland (Finland Distinguished Professor Programme, project No. 127097) and the Walter and Andrée de Nottbeck Foundation. We thank Anne-Mari Luhtanen and Chris Hulatt for their help in the field and laboratory. Tvärminne Zoological Station, South Ostrobothnia and North Ostrobothnia Centres for Economic Development Transport and the Environment, and the Kiviniemi Association of Finnish Lifeboat Institution are acknowledged for invaluable logistic support in river transect sampling.

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Authors and Affiliations

  1. Marine Research Centre, Finnish Environment Institute (SYKE), Helsinki, Finland

    Hermanni Kaartokallio, Eero Asmala, Riitta Autio & David N. Thomas

  2. Department of Bioscience, Aarhus University, Roskilde, Denmark

    Eero Asmala

  3. School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, UK

    David N. Thomas

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  1. Hermanni Kaartokallio
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  2. Eero Asmala
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Correspondence to Hermanni Kaartokallio.

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This article is part of the special issue ‘Carbon Cycling in Aquatic Ecosystems’

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Kaartokallio, H., Asmala, E., Autio, R. et al. Bacterial production, abundance and cell properties in boreal estuaries: relation to dissolved organic matter quantity and quality. Aquat Sci 78, 525–540 (2016). https://doi.org/10.1007/s00027-015-0449-9

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