The Effects of Host Age and Spatial Location on Bacterial Community Composition in the English Oak Tree (Quercus Robur)

The Effects of Host Age and Spatial Location on Bacterial Community Composition in the English Oak Tree (Quercus Robur)

Environmental Microbiology Reports (2016) 8(5), 649–658 doi:10.1111/1758-2229.12418 The effects of host age and spatial location on bacterial community composition in the English Oak tree (Quercus robur) Meaden S.,1* Metcalf C.J.E.2,3 and Koskella B.4 poor understanding of which mechanisms shape the 1College of Life and Environmental Sciences, University plant-associated microbial community or how this might of Exeter, Penryn Campus, TR109FE, United Kingdom. in-turn influence host traits. Furthermore, although plant 2Department of Ecology and Evolutionary Biology, microbiome research has primarily focused on the below Princeton University, Princeton, USA. ground portion of the plant (the rhizosphere), knowledge 3Fogarty International Center, National Institute of of the phylloplane (the microbial composition of leaves) Health, Bethesda, Maryland, USA. is increasing (Lindow and Brandl, 2003; Vorholt, 2012), 4Department of Integrative Biology, University of demonstrating an equally important role in shaping plant California, Berkeley, 94720, USA. phenotype. Still less is known regarding the microbial composition of other organs, with distinct communities Summary reported across tissues within the host, often playing a more important role than biogeography (Ottesen et al., Drivers of bacterial community assemblages associ- 2013; Leff et al., 2014; Coleman-Derr et al., 2016). For ated with plants are diverse and include biotic fac- tree species in particular, the dermosphere (bark associ- tors, such as competitors and host traits, and abiotic ated microbial community, (Lambais et al., 2014) may factors, including environmental conditions and dis- be particularly important given that bacterial pathogens persal mechanisms. We examine the roles of spatial often invade the host through wounds in the bark (Tattar, distribution and host size, as an approximation for 2012; Misas-Villamil et al., 2013). This variation among age, in shaping the microbiome associated with tissues mirrors what is observed in other long-lived Quercus robur woody tissue using culture- hosts, including humans, where data is most abundant; independent 16S rRNA gene amplicon sequencing. In distinct bacterial communities have been isolated from addition to providing a baseline survey of the Q. different skin sites (Grice et al., 2009) and these differ- robur microbiome, we screened for the pathogen of ences appear stable over time (Costello et al., 2009). acute oak decline. Our results suggest that age is a Such variation is also likely to exist across individual predictor of bacterial community composition, dem- plant microbiomes given that they can be heritable onstrating a surprising negative correlation between (Peiffer et al., 2013), shaped by host genetics (Boden- tree age and alpha diversity. We find no signature of hausen et al., 2014; Beckers et al., 2016), and play dispersal limitation within the Wytham Woods plot functional roles that include sensitizing the plant immune sampled. Together, these results provide evidence for niche-based hypotheses of community assembly and system (Pieterse et al., 2014). the importance of tree age in bacterial community The root-associated microbiomes of healthy Arabidop- structure, as well as highlighting that caution must sis plants are arguably the best understood plant micro- be applied when diagnosing dysbiosis in a long-lived biome (Lundberg et al., 2012) with the mechanisms plant host. behind host regulation recently coming to light (Lebeis et al., 2015). However, many more non-model plant spe- cies have had their microbiomes characterized. For example, a number of studies have explored the nature Introduction of tree microbiomes, providing baseline taxonomic sur- Many lines of evidence suggest that microbes are cru- veys and assessing the drivers of community composi- cial for plant health and function (Kim et al., 2011; tion, typically contrasting host traits with climatic or Berendsen et al., 2012), and yet we have a relatively geographic variables. Many of these studies find a strong effect of host phylogeny on the bacterial commu- Received 14 October, 2015; accepted 8 April, 2016. *For corre- nity, with a greater effect of tree species than geographic spondence. E-mail [email protected]; Tel. 15103457086. distance, even across continents (Redford et al., 2010; VC 2016 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 650 S. Meaden, C. J. E. Metcalf and B. Koskella Lambais et al., 2014). Similarly, in a tropical environment biome as they age (Tarpy et al., 2015) and in a wild bird, in Malaysia, Kim et al. (Kim et al., 2012) found a strong Rissa tridactyla, chicks harbor a greater diversity of bac- signal of host phylogeny on bacterial community compo- teria than adults (van Dongen et al., 2013). In plants, sition. Functional host traits such as growth rate and bacterial diversity can be highest on younger leaves in leaf mass have also been demonstrated as key drivers lettuces (Dees et al., 2015), however the evidence is of composition, alongside phylogeny (Kembel et al., mixed as tree-associated bacterial communities can be 2014). In contrast, Finkel et al. (Finkel et al., 2012) strongly influenced by season (Penuelas~ et al., 2012). found trees of the same species in a different desert In this study we describe and explore the bacterial locations host distinct microbial communities. Given composition of Q.robur tree cores in a well-studied UK these conflicting results across the scales examined, it forest, Wytham Woods, in order to answer three key is unclear whether phylloplane microbiomes are subject questions: firstly, what are the typical bacterial taxa to niche-based or neutral models of community associated with this Woodland site; secondly, does geo- assembly. graphic distance affect dispersal, such that there is a Specifically, the roles of dispersal and immigration, in spatial pattern of community composition and distance combination with ecological selection and drift (Vellend, between trees; and thirdly, is Q. robur host age or loca- 2010), have been the focus of a number of theoretical tion important in structuring bacterial communities. To models of community assembly, many of which are answer these questions, we first describe the tree- applicable to microbes (Sloan et al., 2006; Nemergut associated microbiota using amplicon sequencing of the et al., 2013). The niche assembly model states that the 16S rDNA gene of 64 trees. Using a long-term woodland dispersal of bacteria is unhindered by physical con- census we then assess correlations between alpha and straints, and all organisms can be found anywhere but it beta diversity and factors such as age and spatial loca- is the environment which selects for their persistence tion. Additionally, we use these data to compare the pre- (de Wit and Bouvier, 2006). Conversely, the dispersal dicted metabolic functionality and screen our dataset for assembly hypothesis states that the biodiversity we the pathogenic clade Brenneria, the causative agent of observe can largely be explained by stochastic local acute oak decline, from which the UK Q. robur popula- extinctions and dispersal-limitation, typified by the idea tion is currently experiencing an epidemic (Denman of island biogeography (Hubbell, 2001; Volkov et al., et al., 2012). This survey presents a unique opportunity 2003). Whilst this is essentially the “niche vs. neutral” to assess the practicality of high throughput sequencing debate, Fierer (Fierer, 2008) provides the nuances of in environmental monitoring. Given the critical impor- the microbial context including the much higher species tance of detecting and preventing the emergence of tree richness and evenness, and the rapidity of species turn- diseases before large-scale spread, a better understand- over typical of most bacterial communities. ing of tree microbiomes offers additional value in The English oak tree, Quercus robur, study system surveillance. provides an opportunity to test these competing hypoth- eses. If microbial community assembly is purely a Experimental Procedures dispersal-driven process, we would predict a positive Study System relationship between tree age and diversity, as older organisms will have experienced more colonization Wytham Woods is one of the most intensively studied events. Such a positive relationship has been demon- tree populations in Europe and undergoes extensive sur- strated for trees and their plant epiphytes and lichens veys every 2 years0020(Butt et al. 2009). As such, it (Flores-Palacios and Garcia-Franco, 2006; Johansson provides a practical system for correlating a vast number et al., 2007), but has not been shown before in tree- of ecological variables and demographic traits and has associated bacterial communities. Alternatively, if the been the source of numerous important papers (Hunter process is strictly niche-driven, older trees could repre- et al., 1997; Morecroft et al., 2003; Butt et al., 2009). sent an alternative environment to smaller trees, favor- The UK Q. robur population is suffering a number of ing proliferation of particular species but not necessarily infectious diseases, collectively known as oak decline. harboring a greater diversity. This comprises chronic oak decline, sudden oak decline As well as

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