Microbial remineralization processes during postspring-bloom with excess phosphate available in the northern Baltic Sea

. 2024 Jul 12 ; 100 (8) : .

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39039015

Grantová podpora
731065 European Commission
2021/03/Y/NZ8/00076 National Science Centre, Poland
GR1540/37-1 DFG CEP - Centrální evidence projektů

The phosphorus (P) concentration is increasing in parts of the Baltic Sea following the spring bloom. The fate of this excess P-pool is an open question, and here we investigate the role of microbial degradation processes in the excess P assimilation phase. During a 17-day-long mesocosm experiment in the southwest Finnish archipelago, we examined nitrogen, phosphorus, and carbon acquiring extracellular enzyme activities in three size fractions (<0.2, 0.2-3, and >3 µm), bacterial abundance, production, community composition, and its predicted metabolic functions. The mesocosms received carbon (C) and nitrogen (N) amendments individually and in combination (NC) to distinguish between heterotrophic and autotrophic processes. Alkaline phosphatase activity occurred mainly in the dissolved form and likely contributed to the excess phosphate conditions together with grazing. At the beginning of the experiment, peptidolytic and glycolytic enzymes were mostly produced by free-living bacteria. However, by the end of the experiment, the NC-treatment induced a shift in peptidolytic and glycolytic activities and degradation of phosphomonoesters toward the particle-associated fraction, likely as a consequence of higher substrate availability. This would potentially promote retention of nutrients in the surface as opposed to sedimentation, but direct sedimentation measurements are needed to verify this hypothesis.

Zobrazit více v PubMed

Allers  E, Gómez-Consarnau  L, Pinhassi  J  et al.  Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ Microbiol. 2007;9:2417–29. PubMed

Allgaier  M, Bruckner  S, Jaspers  E  et al.  Intra- and inter-lake variability of free-living and particle-associated actinobacteria communities. Environ Microbiol. 2007;9:2728–41. PubMed

Allison  SD, Lu  L, Kent  AG  et al.  Extracellular enzyme production and cheating in Pseudomonas fluorescens depend on diffusion rates. Front Microbiol. 2014;5. 10.3389/fmicb.2014.00169. PubMed DOI PMC

Azúa  I, Unanue  M, Ayo  B  et al.  Influence of organic matter quality in the cleavage of polymers by marine bacterial communities. J Plankton Res. 2003;25:1451–60.

Baltar  F. Watch out for the "living dead": cell-free enzymes and their fate. Front Microbiol. 2018;8. PubMed PMC

Baltar  F, Arístegui  J, Gasol  JM  et al.  High dissolved extracellular enzymatic activity in the deep central Atlantic Ocean. Aquat Microb Ecol. 2010;58:287–302.

Baltar  F, Legrand  C, Pinhassi  J.  Cell-free extracellular enzymatic activity is linked to seasonal temperature changes: a case study in the Baltic Sea. Biogeosciences. 2016;13:2815–21.

Baltar  F, de Corte  D, Yokokawa  T.  Bacterial stress and mortality may be a source of cell-free enzymatic activity in the marine environment. Microbes Environ. 2019;34:83–8. PubMed PMC

Barbera  P.  EPA-ng: efficient probabilistic assignment for DNA sequences. V.0.3.8. GitHub, 2019. https://github.com/pierrebarbera/epa-ng (1 March 2023, date last accessed).

Barbera  P, Kozlov  AM, Czech  L  et al.  EPA-ng: massively parallel evolutionary placement of genetic sequences. Syst Biol. 2019;68:365–9. PubMed PMC

Bashenkhaeva  MV, Galachyants  YP, Khanaev  IV  et al.  Comparative analysis of free-living and particle-associated bacterial communities of Lake Baikal during the ice-covered period. J Great Lakes Res. 2020;46:508–18.

Bochdansky  AB, Puskaric  S, Herndl  GJ.  Influence of zooplankton grazing on free dissolved enzymes in the sea. Mar Ecol Prog Ser. 1995;121:53–63.

Bochdansky  AB, Clouse  MA, Herndl  GJ.  Dragon kings of the deep sea: marine particles deviate markedly from the common number-size spectrum. Sci Rep. 2016;6. 10.1038/srep22633. PubMed DOI PMC

Boyd  P, Trull  T.  Understanding the export of biogenic particles in oceanic waters: is there consensus?. Prog Oceanogr. 2007;72:276–312.

Bunse  C, Bertos-Fortis  M, Sassenhagen  I  et al.  Spatio-temporal interdependence of bacteria and phytoplankton during a Baltic Sea spring bloom. Front Microbiol. 2016;7. 10.3389/fmicb.2016.00517. PubMed DOI PMC

Bunse  C, Israelsson  S, Baltar  F  et al.  High frequency multi-year variability in Baltic Sea microbial plankton stocks and activities. Front Microbiol. 2019;9. 10.3389/fmicb.2018.03296. PubMed DOI PMC

Callahan  BJ, McMurdie  PJ, Rosen  MJ  et al.  DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3. PubMed PMC

Camarena-Gómez  MT, Ruiz-González  C, Piiparinen  J  et al.  Bacterioplankton dynamics driven by interannual and spatial variation indiatom and dinoflagellate spring bloom communities in the Baltic Sea. Limnol Oceanogr. 2020;66:255–271.

Cho  BC, Azam  F.  Major role of bacteria in biogeochemical fluxes in the ocean's interior. Nature. 1988;332:441.

Chróst  RJ.  Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In: Chróst  R.J. (ed.), Microbial Enzymes in Aquatic Environments. Brock/Springer Series in Contemporary Bioscience. New York: Springer, 1991.

Chrzanowski  TH, Kyle  M.  Ratios of carbon, nitrogen and phosphorus in Pseudomonas fluorescens as a model for bacterial element ratios and nutrient regeneration. Aquat Microb Ecol. 1996;10:115–22.

Delmont  TO, Hammar  KM, Ducklow  HW  et al.  Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front Microbiol. 2014;5. 10.3389/fmicb.2014.00646. PubMed DOI PMC

Diepenbroek  M, Glöckner  F, Grobe  P  et al.  Towards an integrated biodiversity and ecological research data management and archiving platform: the German Federation for the Curation of Biological Data (GFBio). In: Plödereder  E, Grunske  L, Schneider  E, Ull  D (eds.), Proceedings of the Informatik 2014–Big Data Komplexität Meistern. GI-edn. Vol. 232. Lecture Notes in Informatics (LNI). Bonn: Köllen Verlag; 2014, 1711–24.

Douglas  GM, Maffei  VJ, Zaneveld  JR  et al.  PICRUSt2 for prediction of metagenome functions. Nat Biotechnol. 2020;38:685–8. PubMed PMC

Eigemann  F, Rahav  E, Grossart  H-P  et al.  Phytoplankton producer species and transformation of released compounds over time define bacterial communities following phytoplankton dissolved organic matter pulses. Appl Environ Microbiol. 2023;89:1–16. PubMed PMC

Eilola  K, Stigebrandt  A.  On the seasonal nitrogen dynamics of the Baltic proper biochemical reactor. J Mar Res. 1999;57:693–713.

Fawcett  SE, Ward  BB. Phytoplankton succession and nitrogen utilization during the development of an upwelling bloom. Mar Ecol Prog Ser. 2011;428:13–31.

Fuhrman  J, Azam  F.  Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar Biol. 1982;66:109–20.

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

González-Gil  S, Keafer  BA, Jovine  RV  et al.  Detection and quantification of alkaline phosphatase in single cells of phosphorus-starved marine phytoplankton. Mar Ecol Prog Ser. 1998;164:21–35.

Grasshoff  K, Ehrhardt  M, Kremling  K.  Methods of Seawater Analysis. 3rd edn. Weinheim: Wiley-VCH, 1999.

Grossart  H-P.  Ecological consequences of bacterioplankton lifestyles: changes in concepts are needed. Environ Microbiol Rep. 2010;2:706–14. PubMed

Grossart  H-P, Ploug  H.  Microbial degradation of organic carbon and nitrogen on diatom aggregates. Limnol Oceanogr. 2001;46:267–77.

Grossart  H-P, Simon  M.  Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquat Microb Ecol. 1998;15:127–40.

Grossart  H-P, Hietanen  S, Ploug  H.  Microbial dynamics on diatom aggregates in Øresund, Denmark. Mar Ecol Prog Ser. 2003;249:69–78.

Grossart  H-P, Engel  A, Arnosti  C  et al.  Microbial dynamics in autotrophic and heterotrophic seawater mesocosms. III. Organic matter fluxes. Aquat Microb Ecol. 2007a;49:143–56.

Grossart  H-P, Tang  KW, Kiørboe  T  et al.  Comparison of cell-specific activity between free-living and attached bacteria using isolates and natural assemblages. FEMS Microbiol Lett. 2007b;266:194–200. PubMed

Grossart  H-P, Van den Wyngaert  S, Kagami  M  et al.  Fungi in aquatic ecosystems. Nat Rev Microbiol. 2019;17:339–54. PubMed

Hansell  DA.  Recalcitrant dissolved organic carbon fractions. Annu Rev Mar Sci. 2013;5:421–45. PubMed

Heiskanen  AS.  Factors governing sedimentation and pelagic nutrient cycles in the northern Baltic Sea. Monogr Boreal Env Res. 1998;8:1–80.

HELCOM 2008 Helsinki Commission (HELCOM) . 2008. Programme for monitoring of eutrophication and its effects. Annex C-11 guidelines concerning bacterioplankton growth determination. In: Manual for Marine Monitoring in the COMBINE Programme of HELCOM. Annex C-1 : 9. Helsinki: HELCOM.

Heldal  M, Norland  S, Fagerbakke  KM  et al.  The elemental composition of bacteria: a signature of growth conditions?. Mar Pollut Bull. 1996;33:3–9.

Hoppe  HG.  Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser. 1983;11:299–308.

Hoppe  HG.  Microbial extracellular enzyme activity: a new key parameter in aquatic ecology. In: Chróst  RJ (ed.), Microbial Enzymes in Aquatic Environments. Brock/Springer Series in Contemporary Bioscience. New York: Springer, 1991.

Hoppe  HG.  Phosphatase activity in the sea. Hydrobiology. 2003;493:187–200.

Hugerth  LW, Larsson  J, Alneberg  J  et al.  Metagenome-assembled genomes uncover a global brackish microbiome. Genome Biol. 2015;16:1–18. PubMed PMC

Inkscape Project . Inkscape. Version 1.3.1. 2020. https://inkscape.org/ (23 October 2023, date last accessed).

Ivančić  I, Pfannkuchen  M, Godrijan  J  et al.  Alkaline phosphatase activity related to phosphorus stress of microphytoplankton in different trophic conditions. Prog Oceanogr. 2016;146:175–86.

Jespersen  AM, Christoffersen  K.  Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol. 1987;109:445–54.

Karner  M, Herndl  GJ.  Extracellular enzymatic activity and secondary production in free-living and marine-snow-associated bacteria. Mar Biol. 1992;113:341–7.

Karner  M, Rassoulzadegan  F.  Extracellular enzyme activity: indications for high short-term variability in a coastal marine ecosystem. Microb Ecol. 1995;30:143–56. PubMed

Kirchman  DL, K´nees  E, Hodson  RE.  Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural systems. Appl Environ Microb. 1985;49:599–607. PubMed PMC

Kirchman  DL.  The uptake of inorganic nutrients by heterotrophic bacteria. Microb Ecol. 1994;28:255–71. PubMed

Kirchman  DL.  The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol. 2002;39:91–100. PubMed

Klindworth  A, Pruesse  E, Schweer  T  et al.  Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1. PubMed PMC

Koch  MS, Kletou  DC, Tursi  R.  Alkaline phosphatase activity of water column fractions and seagrass in a tropical carbonate estuary, Florida Bay. Estuar Coast Shelf Sci. 2009;83:403–13.

Koistinen  J, Sjöblom  M, Spilling  K.  Determining inorganic and organic phosphorus. In: Spilling  K (ed.), Biofuels from Algae. New York: Human Press, 2017, 87–94.

Köster  J, Rahmann  S.  Snakemake−a scalable bioinformatics workflow engine. Bioinformatics. 2012;28:2520–2. PubMed

Lapébie  P, Lombard  V, Drula  E  et al.  Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat Commun. 2019;10:2043. PubMed PMC

Length  R.  emmeans: estimated Marginal Means, aka Least-squares Means. R package version 1.9.0. CRAN, 2023. https://CRAN.R-project.org/package=emmeans.

Lignell  R, Hoikkala  L, Lahtinen  T.  Effects of inorganic nutrients, glucose and solar radiation on bacterial growth and exploitation of dissolved organic carbon and nitrogen in the northern Baltic Sea. Aquat Microb Ecol. 2008;51:209–221.

Lilover  M-J, Stips  A.  The variability of parameters controlling the cyanobacteria bloom biomass in the Baltic Sea. J Mar Syst. 2008;74:S108–15.

Lips  I, Lips  U.  The importance of mesodinium rubrum at post-spring bloom nutrient and phytoplankton dynamics in the vertically stratified Baltic Sea. Front Mar Sci. 2017;4. 10.3389/fmars.2017.00407. DOI

Luo  H, Benner  R, Long  RA  et al.  Subcellular localization of marine bacterial alkaline phosphatases. Proc Natl Acad Sci. 2009;106:21219–23. PubMed PMC

Lyons  MM, Dobbs  FC.  Differential utilization of carbon substrates by aggregate-associated and water-associated heterotrophic bacterial communities. Hydrobiologia. 2012;686:181–193.

Mahaffey  C, Reynolds  S, Davis  CE  et al.  Alkaline phosphatase activity in the subtropical ocean: insights from nutrient, dust and trace metal addition experiments. Front Mar Sci. 2014;1. 10.3389/fmars.2014.00073. DOI

Malfatti  F, Turk  V, Tinta  T  et al.  Microbial mechanisms coupling carbon and phosphorus cycles in phosphorus-limited northern Adriatic Sea. Sci Total Environ. 2014;470–471:1173–83. PubMed

Middelboe  M, Sondergaard  M, Letarte  Y  et al.  Attached and free-living bacteria: production and polymer hydrolysis during a diatom bloom. Microb Ecol. 1995;29:231–48. PubMed

Mohit  V, Archambault  P, Toupoint  N  et al.  Phylogenetic differences in attached and free-living bacterial communities in a temperate coastal lagoon during summer, revealed via high-throughput 16S rRNA gene sequencing. Appl Environ Microbiol. 2014;80:2071–83. PubMed PMC

Murray  AE, Arnosti  C, De La Rocha  CL  et al.  Microbial dynamics in autotrophic and heterotrophic seawater mesocosms. II. Bacterioplankton community structure and hydrolytic enzyme activities. Aquat Microb Ecol. 2007;49:123–41.

Nausch  M.  Alkaline phosphatase activities and the relationship to inorganic phosphate in the Pomeranian Bight (southern Baltic Sea). Aquat Microb Ecol. 1998;16:87–94. PubMed

Nausch  M.  Experimental evidence for interactions between bacterial peptidase and alkaline phosphatase activity in the Baltic Sea. Aquat Ecol. 2000;34:331–43.

Nausch  M, Nausch  G.  Bacterial utilisation of phosphorus pools after nitrogen and carbon amendment and its relation to alkaline phosphatase activity. Aquat Microb Ecol. 2004;37:237–45.

Nausch  M, Pollehne  F, Kerstan  E.  Extracellular enzyme activities in relation to hydrodynamics in the Pomeranian Bight (southern Baltic Sea). Microb Ecol. 1998;36:251–8. PubMed

Nausch  M, Achterberg  EP, Bach  LT  et al.  Concentrations and uptake of dissolved organic phosphorus compounds in the Baltic Sea. Front Mar Sci. 2018;5:386.

Nercessian  O, Noyes  E, Kalyuzhnaya  MG  et al.  Bacterial populations active in metabolism of C1 compounds in the sediment of Lake Washington, a freshwater lake. Appl Environ Microbiol. 2005;71:6885–99. PubMed PMC

Niemi  Å.  Blue-green algal blooms and N:P ratio in the Baltic Sea. Acta Botanica Fennica. 1979;110:57–61.

Norland  S.  The relationship between biomass and volume of bacteria. In: Kemp  PF, Cole  JJ, Sherr  BF, Sherr  EB (eds.), Handbook of Methods in Aquatic Microbial Ecology. Boca Raton: CRC Press, 1993, 303–7.

Pinheiro  J, Bates  D, R Core Team . nlme: linear and nonlinear mixed effects models_. R package version 3.1-162. CRAN, 2023. https://CRAN.R-project.org/package=nlme.

Piwosz  K, Salcher  MM, Zeder  M  et al.  Seasonal dynamics and activity of typical freshwater bacteria in brackish waters of the Gulf of Gdańsk. Limnol Oceanogr. 2013;58:817–26.

Ploug  H, Grossart  H-P.  Bacterial growth and grazing on diatom aggregates: respiratory carbon turnover as a function of aggregate size and sinking velocity. Limnol Oceanogr. 2000;45:1467–75.

R Core Team . R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing, 2022.

Raateoja  M, Kuosa  H, Hällfors  S.  Fate of excess phosphorus in the Baltic Sea: a real driving force for cyanobacterial blooms?. J Sea Res. 2011;65:315–21.

Rahm  L, Jönsson  A, Wulff  F.  Nitrogen fixation in the Baltic proper: an empirical study. J Mar Syst. 2000;25:239–48.

Ramin  KI, Allison  SD.  Bacterial tradeoffs in growth rate and extracellular enzymes. Front Microbiol. 2019;10. 10.3389/fmicb.2019.02956. PubMed DOI PMC

Redfield  AC.  The biological control of chemical factors in the environment. Am Sci. 1958;64:205–21. PubMed

Reintjes  G, Heins  A, Wang  C  et al.  Abundance and composition of particles and their attached microbiomes along an Atlantic Meridional Transect. Front Mar Sci. 2023;10. 10.3389/fmars.2023.1051510. DOI

Rengefors  K, Pettersson  K, Blenckner  T  et al.  Species-specific alkaline phosphatase activity in freshwater spring phytoplankton: application of a novel method. J Plankton Res. 2001;23:435–43.

Rieck  A, Herlemann  DPR, Jürgens  K  et al.  Particle-associated differ from free-living bacteria in surface waters of the Baltic Sea. Front Microbiol. 2015;6. 10.3389/fmicb.2015.01297. PubMed DOI PMC

Salazar-Alekseyeva  K, Herndl  GJ, Baltar  F.  Release of cell-free enzymes by marine pelagic fungal strains. Front Fungal Biol. 4;2023. 10.3389/ffunb.2023.1209265. PubMed DOI PMC

Salerno  M, Stoecker  DK.  Ectocellular glucosidase and peptidase activity of the mixotrophic dinoflagellate Prorocentrum minimum (Dinophyceae). J Phycol. 2009;45:34–45. PubMed

Salonen  K.  A versatile method for the rapid and accurate determination of carbon by high temperature combustion. Limnol Oceanogr. 1979;24:177–83.

Sharp  JH, Peltzer  ET, Alperin  MJ  et al.  Measurement of dissolved organic carbon and nitrogen in natural waters: procedures subgroup report. Mar Chem. 1993;41:37–49.

Sherr  BF, Sherr  EB, Fallon  RD.  Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. Appl Environ Microbiol. 1987;53:958–65. PubMed PMC

Simon  M, Azam  F.  Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser. 1989;51:201–13.

Simon  M, Grossart  H-P, Schweitzer  B  et al.  Microbial ecology of organic aggregates in aquatic ecosystems. Aquat Microb Ecol. 2002;28:175–211.

Smith  DC, Azam  F.  A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs. 1992;6:107–14.

Smith  DC, Simon  M, Alldredge  AL  et al.  Intense hydrolytic enzyme activity on marine aggregates and implication for rapid particle dissolution. Nature. 1992;359:139–41.

Solórzano  L, Sharp  JH.  Determination of total dissolved phosphorus and particulate phosphorus in natural waters. Limnol Oceanogr. 1980;25:754–8.

Spilling  K, Olli  K, Lehtoranta  J  et al.  Shifting diatom–dinoflagellate dominance during spring bloom in the Baltic Sea and its potential effects on biogeochemical cycling. Front Mar Sci. 2018;5. 10.3389/fmars.2018.00327. DOI

Spilling  K, Piiparinen  J, Achterberg  EP  et al.  Extracellular enzyme activity in the coastal upwelling system off Peru: a mesocosm experiment. Biogeosciences. 2023;20:1605–19.

Spilling  K, Vanharanta  M, Santoro  M  et al.  Effects of excess phosphate on a coastal plankton community. Biorxiv. 2024. 10.1101/2024.02.05.576994. DOI

Steen  AD, Arnosti  C.  Long lifetimes of β-glucosidase, leucine aminopeptidase, and phosphatase in Arctic seawater. Mar Chem. 2011;123:127–32.

Steinberg  DK, van Mooy  BAS, Buesseler  KO  et al.  Bacterial vs. zooplankton control of sinking particle flux in the ocean's twilight zone. Limnol Oceanogr. 2008;253:1327–38.

Strojsová  E, Vrba  J, Nedoma  J  et al.  Seasonal study of extracellular phosphatase expression in the phytoplankton of a eutrophic reservoir. Eur J Phycol. 2003;38:295–306.

Tada  Y, Grossart  H-P.  Community shifts of actively growing lake bacteria after N-acetyl-glucosamine addition: improving the BrdU-FACS method. ISME J. 2014;8:441–54. PubMed PMC

Tamelander  T, Heiskanen  AS.  Effects of spring bloom phytoplankton dynamics and hydrography on the composition of settling material in the coastal northern Baltic Sea. J Mar Syst. 2004;52:217–34.

Thingstad  TF, Bellerby  RGJ, Bratbak  G  et al.  Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature. 2008;455:387–90. PubMed

Thomson  B, Wenley  J, Currie  K  et al.  Resolving the paradox: continuous cell-free alkaline phosphatase activity despite high phosphate concentrations. Mar Chem. 2019;214:103671.

Traving  SJ, Balmonte  JP, Seale  D  et al.  On single-cell enzyme assays in marine microbial ecology and biogeochemistry. Front Mar Sci Sec Aquat Microbiol. 2022;9. 10.3389/fmars.2022.846656. DOI

Traving  SJ, Thygesen  UH, Riemann  L  et al.  A model of extracellular enzymes in free-living microbes: which strategy pays off?. Appl Environ Microb. 2015;81:7385–93. PubMed PMC

Vadstein  O, Olsen  LM, Busch  A  et al.  Is phosphorus limitation of lanktonic heterotrophic bacteria and accumulation of degradable DOC a normal phenomenon in phosphorus-limited systems? A microcosm study. FEMS Microbiol Ecol. 2003;46:307–16. PubMed

Vahtera  E, Conley  DJ, Gustafsson  BG  et al.  Internal ecosystem feedback enhance nitrogen-fixing cyanobacteria blooms and complicate management in the Baltic Sea. Ambio. 2007;36:186–94. PubMed

Vanharanta  M, Spilling  K.  The uptake of excess phosphate at low inorganic N:P ratio in a coastal sea afflicted with eutrophication. Mar Ecol Prog Ser. 2023;718:23–37.

Vanharanta  M, Santoro  M, Villena-Alemany  C  et al.  Effect of decreasing inorganic N:P ratio on the plankton community—INN:PP. PANGAEA. 2024. 10.1594/PANGAEA.966040. DOI

Villalba  LA, Karnatak  R, Grossart  H-P  et al.  Flexible habitat choice of pelagic bacteria increases system stability and energy flow through the microbial loop. Limnol Oceanogr. 2022;67:1402–15.

Villena-Alemany  C, Mujakić  I, Fecskeová  LK  et al.  Phenology and ecological role of aerobic anoxygenic phototrophs in freshwaters. Microbiome. 2024;12:65. PubMed PMC

Wickham  H.  GGplot2: Elegant Graphics for Data Analysis. New York: Springer, 2016.

Ylla  I, Romaní  AM, Sabater  S.  Labile and recalcitrant organic matter utilization by river biofilm under increasing water temperature. Microb Ecol. 2012;64:593–604. PubMed

Zhao  L, Brugel  S, Ramasamy  KP  et al.  Bacterial community responses to planktonic and terrestrial substrates in coastal northern Baltic Sea. Front Mar Sci. 2023;10. 10.3389/fmars.2023.1130855. DOI

Ziervogel  K, Arnosti  C.  Polysaccharide hydrolysis in aggregates and free enzyme activity in aggregate-free seawater from the north-eastern Gulf of Mexico. Environ Microbiol. 2008;10:289–99. PubMed

Ziervogel  K, Steen  AD, Arnosti  C.  Changes in the spectrum and rates of extracellular enzyme activities in seawater following aggregate formation. Biogeosciences. 2010;7:1007–15.

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace