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Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress

The ISME Journal (2018) | Download Citation

Abstract

Seagrasses thrive in anoxic sediments where sulphide can accumulate to phytotoxic levels. So how do seagrasses persist in this environment? Here, we propose that radial oxygen loss (ROL) from actively growing root tips protects seagrasses from sulphide intrusion not only by abiotically oxidising sulphides in the rhizosphere of young roots, but also by influencing the abundance and spatial distribution of sulphate-reducing and sulphide-oxidising bacteria. We used a novel multifaceted approach combining imaging techniques (confocal fluorescence in situ hybridisation, oxygen planar optodes, and sulphide diffusive gradients in thin films) with microbial community profiling to build a complete picture of the microenvironment of growing roots of the seagrasses Halophila ovalis and Zostera muelleri. ROL was restricted to young root tips, indicating that seagrasses will have limited ability to influence sulphide oxidation in bulk sediments. On the microscale, however, ROL corresponded with decreased abundance of potential sulphate-reducing bacteria and decreased sulphide concentrations in the rhizosphere surrounding young roots. Furthermore, roots leaking oxygen had a higher abundance of sulphide-oxidising cable bacteria; which is the first direct observation of these bacteria on seagrass roots. Thus, ROL may enhance both abiotic and bacterial sulphide oxidation and restrict bacterial sulphide production around vulnerable roots, thereby helping seagrasses to colonise sulphide-rich anoxic sediments.

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Acknowledgements

Thanks to Morten Larsen and Adam Kessler for their advice in building and optimising the oxygen-optode system and Hannes Schmidt for advice in FISH protocols, as well as PWIS and the PP for many fruitful discussions. We thank the anonymous reviewers whose detailed comments helped improve and clarify this manuscript. We acknowledge the use of the services and facilities of AGRF as well as the facilities, and the scientific and technical assistance of the Australian Microscopy & Microanalysis Research Facility at the Centre for Microscopy, Characterisation & Analysis, The University of Western Australia, a facility funded by the University, State and Commonwealth Governments. Graduate Women WA provided financial support for BCM. Megan Ryan is funded by an ARC Future Fellowship (FT140100103) and Gary Kendrick by two ARC Linkage Grants that also funded the 16 S rRNA sequencing (LP130100918, LP130100155). William Bennett was funded by an ARC Discovery Early Career Researcher Award (DE140100056).

Author information

Affiliations

  1. School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    • Belinda C. Martin
    • , Ylva S. Olsen
    •  & Gary A. Kendrick
  2. The UWA Oceans Institute, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    • Belinda C. Martin
    • , Ylva S. Olsen
    •  & Gary A. Kendrick
  3. Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    • Jeremy Bougoure
    •  & Timothy D. Colmer
  4. School of Agriculture and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    • Megan H. Ryan
  5. Environmental Futures Research Institute, Griffith University, Parklands Drive, Southport, QLD, 4215, Australia

    • William W. Bennett
  6. Ooid Scientific Graphics and Editing, White Gum Valley, WA, 6163, Australia

    • Belinda C. Martin
    •  & Natalie K. Joyce

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Contributions

BCM: study design and conception, method development, data collection data analysis, and drafting manuscript. JB: study design and conception, method development, and drafting manuscript. MR: drafting manuscript. WB: method development, data analysis, and drafting manuscript. TC: method development and drafting of manuscript. NJ: method development and drafting of manuscript. YO: method development, data analysis, and drafting manuscript. GK: study design and conception and drafting manuscript. All authors approved the final manuscript.

Conflict of interest

All authors declare they have no affiliations with or involvement in any organisation or entity with any financial interest or non-financial interest in the work described.

Corresponding author

Correspondence to Belinda C. Martin.

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https://doi.org/10.1038/s41396-018-0308-5