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

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 sul...

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Veröffentlicht in:The ISME Journal 2019-03, Vol.13 (3), p.707-719
Hauptverfasser: Martin, Belinda C., Bougoure, Jeremy, Ryan, Megan H., Bennett, William W., Colmer, Timothy D., Joyce, Natalie K., Olsen, Ylva S., Kendrick, Gary A.
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container_issue 3
container_start_page 707
container_title The ISME Journal
container_volume 13
creator Martin, Belinda C.
Bougoure, Jeremy
Ryan, Megan H.
Bennett, William W.
Colmer, Timothy D.
Joyce, Natalie K.
Olsen, Ylva S.
Kendrick, Gary A.
description 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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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. 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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. 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subjects 14/19
14/32
14/34
14/63
38/23
38/77
631/326/171
631/449/2668
Abundance
Bacteria
Bacteria - classification
Bacteria - genetics
Bacteria - metabolism
Biodiversity
Biomedical and Life Sciences
Ecology
Evolutionary Biology
Fluorescence
Geologic Sediments - chemistry
Grasses
Hybridization
Hydrocharitaceae - microbiology
Hydrocharitaceae - physiology
Imaging techniques
Intrusion
Life Sciences
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Microorganisms
Oxidation
Oxidation-Reduction
Oxygen
Oxygen - metabolism
Plant Roots - microbiology
Plant Roots - physiology
Protective coatings
Rhizosphere
Roots
Seagrasses
Sediments
Spatial distribution
Stress, Physiological
Sulfate reduction
Sulfate-reducing bacteria
Sulfates
Sulfides
Sulfides - metabolism
Thin films
Tips
Zosteraceae - microbiology
Zosteraceae - physiology
title Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress
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