IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0251643.html
   My bibliography  Save this article

Combining SIMS and mechanistic modelling to reveal nutrient kinetics in an algal-bacterial mutualism

Author

Listed:
  • Hannah Laeverenz Schlogelhofer
  • François J Peaudecerf
  • Freddy Bunbury
  • Martin J Whitehouse
  • Rachel A Foster
  • Alison G Smith
  • Ottavio A Croze

Abstract

Microbial communities are of considerable significance for biogeochemical processes, for the health of both animals and plants, and for biotechnological purposes. A key feature of microbial interactions is the exchange of nutrients between cells. Isotope labelling followed by analysis with secondary ion mass spectrometry (SIMS) can identify nutrient fluxes and heterogeneity of substrate utilisation on a single cell level. Here we present a novel approach that combines SIMS experiments with mechanistic modelling to reveal otherwise inaccessible nutrient kinetics. The method is applied to study the onset of a synthetic mutualistic partnership between a vitamin B12-dependent mutant of the alga Chlamydomonas reinhardtii and the B12-producing, heterotrophic bacterium Mesorhizobium japonicum, which is supported by algal photosynthesis. Results suggest that an initial pool of fixed carbon delays the onset of mutualistic cross-feeding; significantly, our approach allows the first quantification of this expected delay. Our method is widely applicable to other microbial systems, and will contribute to furthering a mechanistic understanding of microbial interactions.

Suggested Citation

  • Hannah Laeverenz Schlogelhofer & François J Peaudecerf & Freddy Bunbury & Martin J Whitehouse & Rachel A Foster & Alison G Smith & Ottavio A Croze, 2021. "Combining SIMS and mechanistic modelling to reveal nutrient kinetics in an algal-bacterial mutualism," PLOS ONE, Public Library of Science, vol. 16(5), pages 1-27, May.
  • Handle: RePEc:plo:pone00:0251643
    DOI: 10.1371/journal.pone.0251643
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0251643
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0251643&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0251643?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Martin T. Croft & Andrew D. Lawrence & Evelyne Raux-Deery & Martin J. Warren & Alison G. Smith, 2005. "Algae acquire vitamin B12 through a symbiotic relationship with bacteria," Nature, Nature, vol. 438(7064), pages 90-93, November.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Kapil Amarnath & Avaneesh V. Narla & Sammy Pontrelli & Jiajia Dong & Jack Reddan & Brian R. Taylor & Tolga Caglar & Julia Schwartzman & Uwe Sauer & Otto X. Cordero & Terence Hwa, 2023. "Stress-induced metabolic exchanges between complementary bacterial types underly a dynamic mechanism of inter-species stress resistance," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Yuxiang Zhao & Zishu Liu & Baofeng Zhang & Jingjie Cai & Xiangwu Yao & Meng Zhang & Ye Deng & Baolan Hu, 2023. "Inter-bacterial mutualism promoted by public goods in a system characterized by deterministic temperature variation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Tandon, Puja & Jin, Qiang, 2017. "Microalgae culture enhancement through key microbial approaches," Renewable and Sustainable Energy Reviews, Elsevier, vol. 80(C), pages 1089-1099.
    4. Xavier Mayali & Ty J. Samo & Jeff A. Kimbrel & Megan M. Morris & Kristina Rolison & Courtney Swink & Christina Ramon & Young-Mo Kim & Nathalie Munoz-Munoz & Carrie Nicora & Sam Purvine & Mary Lipton &, 2023. "Single-cell isotope tracing reveals functional guilds of bacteria associated with the diatom Phaeodactylum tricornutum," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Robab Salami & Masoumeh Kordi & Parisa Bolouri & Nasser Delangiz & Behnam Asgari Lajayer, 2021. "Algae-Based Biorefinery as a Sustainable Renewable Resource," Circular Economy and Sustainability,, Springer.
    6. Taelman, Sue Ellen & De Meester, Steven & Van Dijk, Wim & da Silva, Vamilson & Dewulf, Jo, 2015. "Environmental sustainability analysis of a protein-rich livestock feed ingredient in The Netherlands: Microalgae production versus soybean import," Resources, Conservation & Recycling, Elsevier, vol. 101(C), pages 61-72.
    7. Corentin Hochart & Lucas Paoli & Hans-Joachim Ruscheweyh & Guillem Salazar & Emilie Boissin & Sarah Romac & Julie Poulain & Guillaume Bourdin & Guillaume Iwankow & Clémentine Moulin & Maren Ziegler & , 2023. "Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Susheel Bhanu Busi & Massimo Bourquin & Stilianos Fodelianakis & Grégoire Michoud & Tyler J. Kohler & Hannes Peter & Paraskevi Pramateftaki & Michail Styllas & Matteo Tolosano & Vincent Staercke & Mar, 2022. "Genomic and metabolic adaptations of biofilms to ecological windows of opportunity in glacier-fed streams," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Zhang, Tian-Yuan & Hu, Hong-Ying & Wu, Yin-Hu & Zhuang, Lin-Lan & Xu, Xue-Qiao & Wang, Xiao-Xiong & Dao, Guo-Hua, 2016. "Promising solutions to solve the bottlenecks in the large-scale cultivation of microalgae for biomass/bioenergy production," Renewable and Sustainable Energy Reviews, Elsevier, vol. 60(C), pages 1602-1614.
    10. Chengyao Xia & Yuqiang Zhao & Lei Zhang & Xu Li & Yang Cheng & Dongming Wang & Changsheng Xu & Mengyi Qi & Jihong Wang & Xiangrui Guo & Xianfeng Ye & Yan Huang & Danyu Shen & Daolong Dou & Hui Cao & Z, 2023. "Myxobacteria restrain Phytophthora invasion by scavenging thiamine in soybean rhizosphere via outer membrane vesicle-secreted thiaminase I," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Kyong Ha Han & Hyun Jung Kim & Zhun Li & Joo Yeon Youn & Kyeong Yoon Kwak & Min Ho Seo & Jinik Hwang & Sang Deuk Lee & Suk Min Yun & Seok Jin Oh & Jong Woo Park & Weol-Ae Lim & Hyeon Ho Shin, 2020. "Effects of Different Nutrient and Trace Metal Concentrations on Growth of the Toxic Dinoflagellate Gymnodinium catenatum Isolated from Korean Coastal Waters," Sustainability, MDPI, vol. 12(12), pages 1-12, June.
    12. Frigon, Jean-Claude & Matteau-Lebrun, Frédérique & Hamani Abdou, Rekia & McGinn, Patrick J. & O’Leary, Stephen J.B. & Guiot, Serge R., 2013. "Screening microalgae strains for their productivity in methane following anaerobic digestion," Applied Energy, Elsevier, vol. 108(C), pages 100-107.
    13. Tawfik, Ahmed & Niaz, Haider & Qadeer, Kinza & Qyyum, Muhammad Abdul & Liu, J. Jay & Lee, Moonyong, 2022. "Valorization of algal cells for biomass and bioenergy production from wastewater: Sustainable strategies, challenges, and techno-economic limitations," Renewable and Sustainable Energy Reviews, Elsevier, vol. 157(C).
    14. Shousong Zhu & Lauren Higa & Antonia Barela & Caitlyn Lee & Yinhua Chen & Zhi-Yan Du, 2023. "Microalgal Consortia for Waste Treatment and Valuable Bioproducts," Energies, MDPI, vol. 16(2), pages 1-23, January.
    15. Nurulfarah Adilah Rosmahadi & Wai-Hong Leong & Hemamalini Rawindran & Yeek-Chia Ho & Mardawani Mohamad & Noraini A. Ghani & Mohammed J. K. Bashir & Anwar Usman & Man-Kee Lam & Jun-Wei Lim, 2021. "Assuaging Microalgal Harvesting Woes via Attached Growth: A Critical Review to Produce Sustainable Microalgal Feedstock," Sustainability, MDPI, vol. 13(20), pages 1-24, October.
    16. Yunyan Deng & Kui Wang & Zhangxi Hu & Ying-Zhong Tang, 2022. "Abundant Species Diversity and Essential Functions of Bacterial Communities Associated with Dinoflagellates as Revealed from Metabarcoding Sequencing for Laboratory-Raised Clonal Cultures," IJERPH, MDPI, vol. 19(8), pages 1-19, April.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0251643. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.