Low Light Availability Alters Root Exudation and Reduces Putative Beneficial Microorganisms in Seagrass Roots
Total Page:16
File Type:pdf, Size:1020Kb
fmicb-08-02667 January 9, 2018 Time: 17:50 # 1 ORIGINAL RESEARCH published: 11 January 2018 doi: 10.3389/fmicb.2017.02667 Low Light Availability Alters Root Exudation and Reduces Putative Beneficial Microorganisms in Seagrass Roots Belinda C. Martin1,2*, Deirdre Gleeson3, John Statton1,2,4, Andre R. Siebers1†, Pauline Grierson1,5, Megan H. Ryan3 and Gary A. Kendrick1,2,4 1 School of Biological Sciences, The University of Western Australia, Crawley, WA, Australia, 2 UWA Oceans Institute, The University of Western Australia, Crawley, WA, Australia, 3 School of Agriculture and Environment, The University of Western Australia, Crawley, WA, Australia, 4 Western Australian Marine Science Institution, Perth, WA, Australia, 5 West Australian Biogeochemistry Centre, School of Biological Sciences, The University of Western Australia, Crawley, WA, Australia Edited by: Seagrass roots host a diverse microbiome that is critical for plant growth and health. Essaid Ait Barka, Composition of microbial communities can be regulated in part by root exudates, but University of Reims Champagne-Ardenne, France the specifics of these interactions in seagrass rhizospheres are still largely unknown. As Reviewed by: light availability controls primary productivity, reduced light may impact root exudation Julien Tremblay, and consequently the composition of the root microbiome. Hence, we analyzed the National Research Council influence of light availability on root exudation and community structure of the root Canada (NRC–CNRC), Canada Nicola Tomasi, microbiome of three co-occurring seagrass species, Halophila ovalis, Halodule uninervis University of Udine, Italy and Cymodocea serrulata. Plants were grown under four light treatments in mesocosms Hannes Schmidt, University of Vienna, Austria for 2 weeks; control (100% surface irradiance (SI), medium (40% SI), low (20% SI) and *Correspondence: fluctuating light (10 days 20% and 4 days 100%). 16S rDNA amplicon sequencing Belinda C. Martin revealed that microbial diversity, composition and predicted function were strongly [email protected] influenced by the presence of seagrass roots, such that root microbiomes were unique † Present address: to each seagrass species. Reduced light availability altered seagrass root exudation, Andre R. Siebers, Department of Aquatic Ecology, as characterized using fluorescence spectroscopy, and altered the composition of EAWAG, Dübendorf, Switzerland seagrass root microbiomes with a reduction in abundance of potentially beneficial microorganisms. Overall, this study highlights the potential for above-ground light Specialty section: This article was submitted to reduction to invoke a cascade of changes from alterations in root exudation to a Plant Microbe Interactions, reduction in putative beneficial microorganisms and, ultimately, confirms the importance a section of the journal Frontiers in Microbiology of the seagrass root environment – a critical, but often overlooked space. Received: 06 September 2017 Keywords: root microbiome, seagrass, exudation, light, dredging, Sulfurimonas, 16S rDNA, PARAFAC-EEM Accepted: 21 December 2017 Published: 11 January 2018 Citation: INTRODUCTION Martin BC, Gleeson D, Statton J, Siebers AR, Grierson P, Ryan MH It has long been established that roots of terrestrial plants are colonized by a diverse assemblage and Kendrick GA (2018) Low Light of microbes that collectively function as a ‘microbiome.’ These microbiomes are critical for Availability Alters Root Exudation plant growth and health via their influence on biogeochemical cycling and nutrient acquisition, and Reduces Putative Beneficial Microorganisms in Seagrass Roots. induction of host defense to pathogens and disease and production of plant growth regulators Front. Microbiol. 8:2667. (see reviews by Reinhold-Hurek et al. (2015) and Alegria Terrazas et al. (2016). Seagrasses, having doi: 10.3389/fmicb.2017.02667 evolved from land plants, are also colonized by a diverse microbial community that are believed Frontiers in Microbiology | www.frontiersin.org 1 January 2018 | Volume 8 | Article 2667 fmicb-08-02667 January 9, 2018 Time: 17:50 # 2 Martin et al. Seagrass Root Microbiomes and Light to carry out metabolic functions important for their hosts Currently, our knowledge of seagrass root exudation rates including nitrogen fixation (Bagwell et al., 2002; Garcias- and composition is limited to a few studies, most from several Bonet et al., 2016), sulfate reduction and oxidation (Küsel decades ago (Brylinsky, 1977; Penhale and Smith, 1977; Wetzel et al., 2006), phosphate solubilisation (Ghosh et al., 2012) and Penhale, 1979; Wood and Hayasaka, 1981; Moriarty et al., and nutrient turnover (Duarte et al., 2005; Trevathan-Tackett 1986; Holmer et al., 2001). These studies highlight the diversity et al., 2017). However, we are still in the early stages in root exudation patterns (composition and concentration) of understanding seagrass–microbe interactions; consequently, among different seagrass species. It has also been shown that whole-organism (seagrass C microbiome) adaptability, metabolic seagrass metabolism shifts under anoxia (Hasler-Sheetal et al., diversity and, therefore, resilience of the seagrass and microbiome 2015), which can lead to increased exudation of carbon from to environmental change remains largely unexplored. roots as fermentation products (Smith et al., 1988). The species- Seagrass meadows provide a multitude of beneficial ecosystem specific nature of root exudation and the change in exudation in services including, habitat structure, carbon sequestration, reduced light could in turn influence the composition of the root primary food sources and protection from coastal erosion microbiome. However, this top-down effect on the microbiome (Orth et al., 2006). Because seagrasses have a relatively high has not yet been investigated. requirement for light (minimal 11% surface irradiance versus The aim of this research was to assess the impact of light 1% for phytoplankton), they are restricted to growing in shallow reduction on root exudation and the root microbiome of three coastal environments, which also makes them vulnerable to tropical seagrasses Halophila ovalis, Halodule uninervis and human and natural activities that can reduce light penetration Cymodocea serrulata. These three species commonly grow in (e.g., eutrophication, dredging and cyclones) (Orth et al., 2006; mixed meadows in the northwest of Western Australia. In a Ralph et al., 2007; Waycott et al., 2009). A reduction in light previous study we found that root exudation in these three species availability reduces photosynthetic performance and therefore was increased when light availability was reduced in a fluctuating impacts negatively on growth, productivity and overall survival pattern (Martin et al., 2017). In the present work, we test if the of the plant (Biber et al., 2009; Yaakub et al., 2014). Seagrasses impact of light reduction also affects the root microbiome of these avoid negative impacts from short-term light reductions by seagrass species through alterations in root exudation and if any modifications to their physiology and metabolism; thus, light variation in the root microbiome among the seagrass species is reduction of more than 1 month may be required to affect growth related to variation in exudation profiles. We selected these three (Longstaff and Dennison, 1999; Ralph et al., 2007; McMahon seagrass species as they all have relatively fast growth rates and et al., 2013). In contrast, microbial communities can respond are quick to respond to environmental disturbance compared to rapidly to disturbance (Allison and Martiny, 2008) and therefore larger seagrass species (Kilminster et al., 2015). We addressed monitoring their composition could prove an effective early three hypotheses: (i) the composition and predicted function of indicator of environmental fluctuations and ecosystem change. the root microbiome will differ among seagrass species and also Composition of root-associated microbial communities is be distinct from the surrounding sediment, (ii) root exudation controlled by factors at several scales, including those arising will be increased by low and/or fluctuating light availability, from interactions with other microbes (e.g., competition, cross- and (iii) microbial composition and predicted function will be feeding) as well as regulated at an environmental (e.g., pH, influenced by light availability, but in a seagrass species-specific temperature) or host level (plant) (Wagner et al., 2016; Widder manner. et al., 2016; Wemheuer et al., 2017). One of the most important ways in which microbial composition can be regulated from the host level in terrestrial plants is via the exudation of MATERIALS AND METHODS compounds from plant roots. Exudates can shape communities that are specific to the plant species or even plant genotype Site Description and Seagrass Collection by selectively stimulating or inhibiting particular microbial Seagrass species were collected from Useless Loop in Shark ◦ 0 ◦ 0 populations (Haichar et al., 2012; Chaparro et al., 2014; Alegria Bay, Western Australia, in May 2015 (26 07 S 113 24 E). Shark Terrazas et al., 2016; Kawasaki et al., 2016; Martin et al., 2016). Bay is a subtropical marine embayment that is characterized This root exudate–microbe interaction has been demonstrated to by phosphorus-limited carbonate sediments and a hyper-salinity some extent for seagrass species. For example, bacteria isolated gradient extending from north (∼36 psu) to south