Floral organs act as environmental filters and interact with pollinators to structure the yellow monkeyflower (Mimulus guttatus) floral microbiome

Abstract

Assembly of microbial communities is the result of neutral and selective processes. However, the relative importance of these processes is still debated. Microbial communities of flowers, in particular, have gained recent attention because of their potential impact to plant fitness and plant‐pollinator interactions. However, the role of selection and dispersal in the assembly of these communities remains poorly understood. Here, we evaluated the role of pollinator‐mediated dispersal on the contribution of neutral and selective processes in the assembly of floral microbiomes of the yellow monkeyflower (Mimulus guttatus). We sampled floral organs from flowers in the presence and absence of pollinators within five different serpentine seeps in CA and obtained 16S amplicon data on the epiphytic bacterial communities. Consistent with strong microenvironment selection within flowers we observed significant differences in community composition across floral organs and only a small effect of geographic distance. Pollinator exposure affected the contribution of environmental selection and depended on the rate and intimacy of interactions with flower visitors. This study provides evidence of the importance of dispersal and within‐flower heterogeneity in shaping epiphytic bacterial communities of flowers, and highlights the complex interplay between pollinator behaviour, environmental selection and additional abiotic factors in shaping the epiphytic bacterial communities of flowers.

Nectar bacteria stimulate pollen germination and bursting to enhance their fitness

“…More direct effects are also possible. Acinetobacter is common on many floral surfaces, including stigmas (52) and is prevalent in seed microbiomes (53), particularly following pollinator visitation. Whether Acinetobacter growth on stigmas affects pollen germination and success in fertilization will also require further study.…”

Spatially explicit depiction of a floral epiphytic bacterial community reveals role for environmental filtering within petals

“…All ASVs with a mean relative abundance of at least 0.001% in VEAL samples, were also present in HETU. These ASVs are from genera commonly found in floral microbiomes, such as Pantoea , Erwinia , Pseudomonas , Acinetobacter , and Rosenbergiella (Aleklett et al, 2014; von Arx et al, 2019; Junker et al, 2011; Rebolleda‐Gómez & Ashman, 2019; Steven et al, 2018). However, 73 (58%) ASVs were found only in HETU samples.…”

“…For example, floral organs differ in their production of volatiles, secondary metabolites, or aqueous exudates that can support microbes (Aleklett et al, 2014; Junker & Keller, 2015; Rebolleda‐Gómez & Ashman, 2019; Steven et al, 2018). Direct evidence in support of these processes is accumulating for floral epiphytic and aqueous nectar communities (e.g., Morris et al, 2020; Rebolleda‐Gómez & Ashman, 2019; Zemenick et al, 2018). However, outside the nectar environment (e.g., Dhami et al, 2018; Vannette et al, 2020; de Vega & Herrera, 2012), no study has attempted to link microbial functional traits to floral habitat variation.…”

“…This approach has accelerated our understanding of composition and functional aspects of nectar microbial communities (e.g., Herrera et al, 2010; Rering et al, 2018), but as far as we know the cultivability of the entire epiphytic community, outside nectar (Morris et al, 2020) has not been determined for any floral organ. While there is much debate over the cultivability of microbial communities including those of plants (Burch et al, 2016; Martiny, 2019; Steen et al, 2019; Yashiro et al, 2011), the diversity of the anthosphere is lower than the phyllosphere or rhizosphere (Abdelfattah et al, 2019; Rebolleda‐Gómez & Ashman, 2019; Wei & Ashman, 2018), and thus it may be possible to cultivate a larger fraction of the whole epiphytic community of a single floral organ, specifically, a petal, providing unparalleled insight into its function.…”

Pollinators mediate floral microbial diversity and microbial network under agrochemical disturbance

“…Our understanding of what governs microbiome assembly in flowers—a highly dynamic niche—has advanced only recently (Aleklett et al, 2014; Vannette, 2020). The identified drivers include, for instance, microbial dispersal mediated by pollinators (Morris et al, 2020; Rebolleda‐Gómez & Ashman, 2019; Vannette & Fukami, 2017), floral traits that can influence niche availability (e.g., flower size, nectar volume) (Vannette et al, 2020) and microbial source pool (e.g., flower abundance; this study), and disturbance imposed by bactericides and fungicides especially in crop plants (Bartlewicz et al, 2016; Schaeffer et al, 2017). Yet, as these different drivers have often been studied independently, we lack a clear view as to how they act together and thus their relative importance in shaping the floral microbiome.…”