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Nitrogen Assimilation Varies Among Clades of Nectar- and Insect-Associated Acinetobacters

  • Environmental Microbiology
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Abstract

Floral nectar is commonly colonized by yeasts and bacteria, whose growth largely depends on their capacity to assimilate nutrient resources, withstand high osmotic pressures, and cope with unbalanced carbon-to-nitrogen ratios. Although the basis of the ecological success of these microbes in the harsh environment of nectar is still poorly understood, it is reasonable to assume that they are efficient nitrogen scavengers that can consume a wide range of nitrogen sources in nectar. Furthermore, it can be hypothesized that phylogenetically closely related strains have more similar phenotypic characteristics than distant relatives. We tested these hypotheses by investigating the growth performance on different nitrogen-rich substrates of a collection of 82 acinetobacters isolated from nectar and honeybees, representing members of five species (Acinetobacter nectaris, A. boissieri, A. apis, and the recently described taxa A. bareti and A. pollinis). We also analyzed possible links between growth performance and phylogenetic affiliation of the isolates, while taking into account their geographical origin. Results demonstrated that the studied isolates could utilize a wide variety of nitrogen sources, including common metabolic by-products of yeasts (e.g., ammonium and urea), and that phylogenetic relatedness was associated with the variation in nitrogen assimilation among the studied acinetobacters. Finally, nutrient source and the origin (sample type and country) of isolates also predicted the ability of the acinetobacters to assimilate nitrogen-rich compounds. Overall, these results demonstrate inter-clade variation in the potential of the acinetobacters as nitrogen scavengers and suggest that nutritional dependences might influence interactions between bacteria and yeasts in floral nectar.

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Data Availability

The nucleotide sequences determined in this work have been deposited in the GenBank/ENA/DDBJ databases under the accession numbers MN315286 to MN315354. All relevant results are included in this paper or available as supplementary materials at the journal’s website.

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Acknowledgments

We thank the members of KU Leuven’s PME&BIM Lab and the Scientia Terrae Research Institute for feedback. The constructive comments from the journal’s editor and four anonymous reviewers are gratefully acknowledged.

Funding

This work was supported by funding from the European Union’s Horizon 2020 research and innovation program (to SA-P, Marie Skłodowska-Curie Grant Agreement No. 742964) and the United States National Science Foundation (DEB 1737758). SA-P acknowledges a “Ramón y Cajal” contract funded by the Spanish Ministry of Science and Innovation [RYC2018-023847-I]. The funders had no role in the preparation of the manuscript or decision to publish.

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Authors and Affiliations

  1. Department of Microbial and Molecular Systems, Laboratory for Process Microbial Ecology and Bioinspirational Management (PME&BIM), KU Leuven, B-3001, Leuven, Belgium

    Sergio Álvarez-Pérez, Ado Van Assche & Bart Lievens

  2. Department of Animal Health, Complutense University of Madrid, 28040, Madrid, Spain

    Sergio Álvarez-Pérez

  3. Center for Ecological Research, Kyoto University, Hirano 2, Otsu, Shiga, 520-2113, Japan

    Kaoru Tsuji

  4. Department of BioSciences, Rice University, Houston, TX, 77005, USA

    Marion Donald

  5. Department of Entomology and Nematology, University of California Davis, Davis, CA, 95616, USA

    Rachel L. Vannette

  6. Estación Biológica de Doñana, CSIC, 41092, Sevilla, Spain

    Carlos M. Herrera

  7. Biology Department, Laboratory of Plant Conservation and Population Biology, KU Leuven, B-3001, Leuven, Belgium

    Hans Jacquemyn

  8. Department of Biology, Stanford University, Stanford, CA, 94305, USA

    Tadashi Fukami

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  1. Sergio Álvarez-Pérez
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  8. Tadashi Fukami
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Contributions

Conceptualization and resources: all authors. Investigation, formal analysis, and data curation: SA-P and AVA. Writing—original draft preparation: SA-P. Writing—review and editing: all authors. Supervision: BL and TF. Funding: SA-P, BL, and TF.

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Correspondence to Sergio Álvarez-Pérez or Bart Lievens.

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Álvarez-Pérez, S., Tsuji, K., Donald, M. et al. Nitrogen Assimilation Varies Among Clades of Nectar- and Insect-Associated Acinetobacters. Microb Ecol 81, 990–1003 (2021). https://doi.org/10.1007/s00248-020-01671-x

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  • DOI: https://doi.org/10.1007/s00248-020-01671-x

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