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Effects of Phosphorus Limitation on the Bioavailability of DOM Released by Marine Heterotrophic Prokaryotes

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Abstract

Heterotrophic prokaryotes (HP) contribute largely to dissolved organic matter (DOM) processing in the ocean, but they also release diverse organic substances. The bioavailability of DOM released by HP under varying environmental conditions has not been fully elucidated. In this study, we investigated the bioavailability of DOM released by a single bacterial strain (Sphingopyxis alaskensis) and 2 natural HP communities grown under P-replete and P-limited conditions. The released DOM (HP-DOM) was used as a substrate for natural HP communities at a coastal site in the Northwestern Mediterranean Sea. We followed changes in HP growth, enzymatic activity, diversity, and community composition together with the consumption of HP-DOM fluorescence (FDOM). HP-DOM produced under P-replete and P-limited conditions promoted significant growth in all incubations. No clear differences in HP-DOM lability released under P-repletion and P-limitation were evidenced based on the HP growth, and P-limitation was not demonstrated to decrease HP-DOM lability. However, HP-DOM supported the growth of diverse HP communities, and P-driven differences in HP-DOM quality were selected for different indicator taxa in the degrading communities. The humic-like fluorescence, commonly considered recalcitrant, was consumed during the incubations when this peak was initially dominating the FDOM pool, and this consumption coincided with higher alkaline phosphatase activity. Taken together, our findings emphasize that HP-DOM lability is dependent on both DOM quality, which is shaped by P availability, and the composition of the consumer community.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author upon request. Sequence data will be uploaded to the EMBL-ENA data repository.

References

  1. Hansell DA (2013) Recalcitrant dissolved organic carbon fractions. Ann Rev Mar Sci 5:421–445. https://doi.org/10.1146/annurev-marine-120710-100757

    Article  PubMed  Google Scholar 

  2. Azam F, Fenchel T, Field J et al (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263. https://doi.org/10.3354/meps010257

    Article  Google Scholar 

  3. Jiao N, Herndl GJ, Hansell DA et al (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8:593–599. https://doi.org/10.1038/nrmicro2386

    Article  CAS  PubMed  Google Scholar 

  4. Legendre L, Rivkin RB, Weinbauer MG et al (2015) The microbial carbon pump concept: Potential biogeochemical significance in the globally changing ocean. Prog Oceanogr 134:432–450. https://doi.org/10.1016/j.pocean.2015.01.008

    Article  Google Scholar 

  5. Jiao N, Azam F (2011) Microbial carbon pump and its significance for carbon sequestration in the ocean. Microbial carbon pump in the ocean. Science/AAAS, Washington, DC

    Chapter  Google Scholar 

  6. Daoud ABA, Tremblay L (2019) HPLC-SEC-FTIR characterization of the dissolved organic matter produced by the microbial carbon pump. Mar Chem 215:103668. https://doi.org/10.1016/j.marchem.2019.103668

    Article  CAS  Google Scholar 

  7. LaBrie R, Péquin B, Fortin St-Gelais N et al (2022) Deep ocean microbial communities produce more stable dissolved organic matter through the succession of rare prokaryotes. Sci Adv 8:eabn0035. https://doi.org/10.1126/sciadv.abn0035

    Article  CAS  PubMed  Google Scholar 

  8. Lechtenfeld OJ, Hertkorn N, Shen Y et al (2015) Marine sequestration of carbon in bacterial metabolites. Nat Commun 6:6711. https://doi.org/10.1038/ncomms7711

    Article  CAS  PubMed  Google Scholar 

  9. Ogawa H (2001) Production of refractory dissolved organic matter by bacteria. Science 292:917–920. https://doi.org/10.1126/science.1057627

    Article  CAS  PubMed  Google Scholar 

  10. Ortega-Retuerta E, Devresse Q, Caparros J et al (2021) Dissolved organic matter released by two marine heterotrophic bacterial strains and its bioavailability for natural prokaryotic communities. Environ Microbiol 23:1363–1378. https://doi.org/10.1111/1462-2920.15306

    Article  CAS  PubMed  Google Scholar 

  11. Osterholz H, Niggemann J, Giebel H-A et al (2015) Inefficient microbial production of refractory dissolved organic matter in the ocean. Nat Commun 6:7422. https://doi.org/10.1038/ncomms8422

    Article  CAS  PubMed  Google Scholar 

  12. Jiao N, Robinson C, Azam F et al (2014) Mechanisms of microbial carbon sequestration in the ocean – future research directions. Biogeosciences 11:5285–5306. https://doi.org/10.5194/bg-11-5285-2014

    Article  Google Scholar 

  13. Alonso-Sáez L, Gasol JM (2007) Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in Northwestern Mediterranean coastal waters. Appl Environ Microbiol 73:3528–3535. https://doi.org/10.1128/AEM.02627-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Krüger K, Chafee M, Ben Francis T et al (2019) In marine Bacteroidetes the bulk of glycan degradation during algae blooms is mediated by few clades using a restricted set of genes. ISME J 13:2800–2816. https://doi.org/10.1038/s41396-019-0476-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. McCarren J, Becker JW, Repeta DJ et al (2010) Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci U S A 107:16420–16427. https://doi.org/10.1073/pnas.1010732107

    Article  PubMed  PubMed Central  Google Scholar 

  16. Sala MM, Ruiz-González C, Borrull E et al (2020) Prokaryotic capability to use organic substrates across the global tropical and subtropical ocean. Front Microbiol 11

  17. Arnosti C, Steen AD, Ziervogel K et al (2011) Latitudinal gradients in degradation of marine dissolved organic carbon. PloS One 6:e28900. https://doi.org/10.1371/journal.pone.0028900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lønborg C, Álvarez-Salgado XA, Letscher RT, Hansell DA (2018) Large stimulation of recalcitrant dissolved organic carbon degradation by increasing ocean temperatures. Front Mar Sci 4:436. https://doi.org/10.3389/fmars.2017.00436

    Article  Google Scholar 

  19. Obernosterer I, Kawasaki N, Benner R (2003) P-limitation of respiration in the Sargasso Sea and uncoupling of bacteria from P-regeneration in size-fractionation experiments. Aquat Microb Ecol 32:229–237. https://doi.org/10.3354/ame032229

    Article  Google Scholar 

  20. Lazzari P, Solidoro C, Salon S, Bolzon G (2016) Spatial variability of phosphate and nitrate in the Mediterranean Sea: a modeling approach. Deep-Sea Res I Oceanogr Res Pap 108:39–52. https://doi.org/10.1016/j.dsr.2015.12.006

    Article  CAS  Google Scholar 

  21. Thingstad TF, Zweifel UL, Rassoulzadegan F (1998) P limitation of heterotrophic bacteria and phytoplankton in the northwest Mediterranean. Limnol Oceanogr 43:88–94. https://doi.org/10.4319/lo.1998.43.1.0088

    Article  CAS  Google Scholar 

  22. Pinhassi J, Gómez-Consarnau L, Alonso-Sáez L et al (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44:241–252. https://doi.org/10.3354/ame044241

    Article  Google Scholar 

  23. Obernosterer I, Herndl G (1995) Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N: P ratio. Mar Ecol Prog Ser 116:247–257. https://doi.org/10.3354/meps116247

    Article  Google Scholar 

  24. Puddu A, Zoppini A, Fazi S et al (2003) Bacterial uptake of DOM released from P-limited phytoplankton. FEMS Microbiol Ecol 46:257–268. https://doi.org/10.1016/S0168-6496(03)00197-1

    Article  CAS  PubMed  Google Scholar 

  25. Romano S, Dittmar T, Bondarev V et al (2014) Exo-metabolome of Pseudovibrio sp. FO-BEG1 analyzed by ultra-high resolution mass spectrometry and the effect of phosphate limitation. PloS One 9:e96038. https://doi.org/10.1371/journal.pone.0096038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bouchachi N, Obernosterer I, Marie B et al (2022) Phosphorus limitation determines the quality of dissolved organic matter released by marine heterotrophic prokaryotes. Limnol Oceanogr Lett n/a. https://doi.org/10.1002/lol2.10287

  27. Thompson SK, Cotner JB (2020) P-limitation drives changes in DOM production by aquatic bacteria. Aquat Microb Ecol 85:35–46. https://doi.org/10.3354/ame01940

    Article  Google Scholar 

  28. Coble PG, Green SA, Blough NV, Gagosian RB (1990) Characterization of dissolved organic matter in the Black Sea by fluorescence spectroscopy. Nature 348:432–435. https://doi.org/10.1038/348432a0

    Article  CAS  Google Scholar 

  29. Yamashita Y, Tanoue E (2008) Production of bio-refractory fluorescent dissolved organic matter in the ocean interior. Nat Geosci 1:579–582. https://doi.org/10.1038/ngeo279

    Article  CAS  Google Scholar 

  30. Catalá TS, Reche I, Fuentes-Lema A et al (2015) Turnover time of fluorescent dissolved organic matter in the dark global ocean. Nat Commun 6:5986. https://doi.org/10.1038/ncomms6986

    Article  CAS  PubMed  Google Scholar 

  31. Jiao N, Cai R, Zheng Q et al (2018) Unveiling the enigma of refractory carbon in the ocean. Natl Sci Rev 5:459–463. https://doi.org/10.1093/nsr/nwy020

    Article  CAS  Google Scholar 

  32. Lønborg C, Álvarez-Salgado XA, Davidson K, Miller AEJ (2009) Production of bioavailable and refractory dissolved organic matter by coastal heterotrophic microbial populations. Estuar Coast Shelf Sci 82:682–688. https://doi.org/10.1016/j.ecss.2009.02.026

    Article  CAS  Google Scholar 

  33. Nieto-Cid M, Álvarez-Salgado XA, Pérez FF (2006) Microbial and photochemical reactivity of fluorescent dissolved organic matter in a coastal upwelling system. Limnol Oceanogr 51:1391–1400. https://doi.org/10.4319/lo.2006.51.3.1391

    Article  CAS  Google Scholar 

  34. Yamashita Y, Tanoue E (2003) Chemical characterization of protein-like fluorophores in DOM in relation to aromatic amino acids. Mar Chem 82:255–271. https://doi.org/10.1016/S0304-4203(03)00073-2

    Article  CAS  Google Scholar 

  35. Lebaron P, Parthuisot N, Catala P (1998) Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems. Appl Environ Microbiol 64:1725–1730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Obernosterer I, Catala P, Lami R et al (2008) Biochemical characteristics and bacterial community structure of the sea surface microlayer in the South Pacific Ocean. Biogeosciences 5:693–705

    Article  CAS  Google Scholar 

  37. Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414. https://doi.org/10.1111/1462-2920.13023

    Article  CAS  PubMed  Google Scholar 

  38. Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Parks DH, Chuvochina M, Waite DW et al (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004. https://doi.org/10.1038/nbt.4229

    Article  CAS  PubMed  Google Scholar 

  40. Kassambara A (2021) rstatix: Pipe-Friendly Framework for Basic Statistical Tests

  41. Oksanen J, Blanchet FG, Friendly M, et al (2020) vegan community ecology package version 2.5–7. November 2020

  42. Roberts DW (2019) labdsv: Ordination and Multivariate Analysis for Ecology

  43. Nieto-Cid M, Álvarez-Salgado XA, Gago J, Pérez FF (2005) DOM fluorescence, a tracer for biogeochemical processes in a coastal upwelling system (NW Iberian Peninsula). Mar Ecol Prog Ser 297:33–50. https://doi.org/10.3354/meps297033

    Article  CAS  Google Scholar 

  44. Romera-Castillo C, Sarmento H, Álvarez-Salgado XA et al (2011) Net production and consumption of fluorescent colored dissolved organic matter by natural bacterial assemblages growing on marine phytoplankton exudates. Appl Environ Microbiol 77:7490–7498. https://doi.org/10.1128/AEM.00200-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Cory RM, Kaplan LA (2012) Biological lability of streamwater fluorescent dissolved organic matter. Limnol Oceanogr 57:1347–1360. https://doi.org/10.4319/lo.2012.57.5.1347

    Article  CAS  Google Scholar 

  46. Varela MM, Rodríguez-Ramos T, Guerrero-Feijóo E, Nieto-Cid M (2020) Changes in activity and community composition shape bacterial responses to size-fractionated marine DOM. Front Microbiol 11:586148. https://doi.org/10.3389/fmicb.2020.586148

    Article  PubMed  PubMed Central  Google Scholar 

  47. Arai K, Wada S, Shimotori K et al (2018) Production and degradation of fluorescent dissolved organic matter derived from bacteria. J Oceanogr 74:39–52. https://doi.org/10.1007/s10872-017-0436-y

    Article  CAS  Google Scholar 

  48. Xie R, Wang Y, Chen Q et al (2020) Coupling between carbon and nitrogen metabolic processes mediated by coastal microbes in Synechococcus-derived organic matter addition incubations. Front Microbiol 11

  49. Lidbury IDEA, Scanlan DJ, Murphy ARJ et al (2022) A widely distributed phosphate-insensitive phosphatase presents a route for rapid organophosphorus remineralization in the biosphere. Proc Natl Acad Sci U S A 119:e2118122119. https://doi.org/10.1073/pnas.2118122119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Noriega-Ortega BE, Wienhausen G, Mentges A et al (2019) Does the chemodiversity of bacterial exometabolomes sustain the chemodiversity of marine dissolved organic matter? Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.00215

  51. Landa M, Cottrell MT, Kirchman DL et al (2014) Phylogenetic and structural response of heterotrophic bacteria to dissolved organic matter of different chemical composition in a continuous culture study. Environ Microbiol 16:1668–1681. https://doi.org/10.1111/1462-2920.12242

    Article  CAS  PubMed  Google Scholar 

  52. Müller O, Seuthe L, Bratbak G, Paulsen ML (2018) Bacterial response to permafrost derived organic matter input in an Arctic Fjord. Front Mar Sci 5

  53. Nelson CE, Carlson CA (2012) Tracking differential incorporation of dissolved organic carbon types among diverse lineages of Sargasso Sea bacterioplankton. Environ Microbiol 14:1500–1516. https://doi.org/10.1111/j.1462-2920.2012.02738.x

    Article  CAS  PubMed  Google Scholar 

  54. Luo H, Benner R, Long RA, Hu J (2009) Subcellular localization of marine bacterial alkaline phosphatases. Proc Natl Acad Sci 106:21219–21223. https://doi.org/10.1073/pnas.0907586106

    Article  PubMed  PubMed Central  Google Scholar 

  55. Xiao X, Guo W, Li X et al Viral lysis alters the optical properties and biological availability of dissolved organic matter derived from Prochlorococcus Picocyanobacteria. Appl Environ Microbiol 87:e02271–20. https://doi.org/10.1128/AEM.02271-20

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Acknowledgements

This work was supported by the Caramba (European Commission, H2020-MSCA-IF-2015-703991), ODISEA (Institut National des Sciences de l’Univers LEFE/CYBER 2019), and MicroPump (Agence Nationale de Recherche ANR-20-CE01-0007) projects to EOR. Flow cytometric analyses were performed at the BioPic cytometry and imaging platform (Sorbonne University/CNRS). The authors thank the crew of R/V “Nereis II” and the technicians of the Banyuls observation service for their assistance in getting Mediterranean Sea samples for the natural communities’ isolation.

Funding

This work was supported by the Caramba (European commission, H2020-MSCA-IF-2015-703991), ODISEA (INSU LEFE/CYBER 2019), and MicroPump (ANR JCJC 2020) projects to EOR.

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Authors and Affiliations

  1. CNRS/Sorbonne Université, UMR7621 Laboratoire d’Océanographie Microbienne, Banyuls sur Mer, France

    Nawal Bouchachi, Ingrid Obernosterer, Cécile Carpaneto Bastos, Franck Li, Lorenzo Scenna, Barbara Marie, Olivier Crispi, Philippe Catala & Eva Ortega-Retuerta

  2. Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy

    Lorenzo Scenna

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  1. Nawal Bouchachi
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  2. Ingrid Obernosterer
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  5. Lorenzo Scenna
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  9. Eva Ortega-Retuerta
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Contributions

NB, EOR, and IO conceived the experimental work. NB, FL, CCB, LS, and EOR performed the experiments, with active contributions from OC, BM, and PC to chemical and biological analyses. NB analyzed the data with contributions from FL, CCB, LS, and EOR. NB wrote the manuscript with significant contributions from IO and EOR. All authors reviewed and approved the final manuscript.

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Correspondence to Nawal Bouchachi or Eva Ortega-Retuerta.

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Bouchachi, N., Obernosterer, I., Carpaneto Bastos, C. et al. Effects of Phosphorus Limitation on the Bioavailability of DOM Released by Marine Heterotrophic Prokaryotes. Microb Ecol 86, 1961–1971 (2023). https://doi.org/10.1007/s00248-023-02201-1

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