Among-Population Variation in Microbial Community Structure in the Floral Nectar of the Bee-Pollinated Forest Herb Pulmonaria officinalis L

Jacquemyn, Hans; Lenaerts, Marijke; Brys, Rein; Willems, Kris; Honnay, Olivier; Lievens, Bart

doi:10.1371/journal.pone.0056917

Cited by 57 publications

(54 citation statements)

References 42 publications

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“…In particular, short generation times and small habitat sizes of microbial species allow community dynamics to be observed for many generations under rigorous experimental control over environmental conditions and species arrival history. In addition, rapidly accumulating knowledge on the natural history of nectar-inhabiting microorganisms [22,[26][27][28][29] enables one to design experiments in which ecological drivers experienced by these species in the field can be simulated and manipulated in the laboratory. Evidence indicates the presence of inhibitive priority effects among some of these nectar-inhabiting species [30] and high sensitivity of these species to ambient temperature [29].…”

Section: Introductionmentioning

confidence: 99%

Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes

2014

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The order of species arrival during community assembly can greatly affect species coexistence, but the strength of these effects, known as priority effects, appears highly variable across species and ecosystems. Furthermore, the causes of this variation remain unclear despite their fundamental importance in understanding species coexistence. Here, we show that one potential cause is environmental variability. In laboratory experiments using nectarinhabiting microorganisms as a model system, we manipulated spatial and temporal variability of temperature, and examined consequences for priority effects. If species arrived sequentially, multiple species coexisted under variable temperature, but not under constant temperature. Temperature variability prevented extinction of late-arriving species that would have been excluded owing to priority effects if temperature had been constant. By contrast, if species arrived simultaneously, species coexisted under both variable and constant temperatures. We propose possible mechanisms underlying these results using a mathematical model that incorporates contrasting effects of microbial species on nectar pH and amino acids. Overall, our findings suggest that understanding consequences of priority effects for species coexistence requires explicit consideration of environmental variability.

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Section: Introductionmentioning

confidence: 99%

Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes

2014

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“…6b), which is less frequently observed in Belgian P. officinalis populations, might account for asymmetrical pollen flow between the morphs in natural populations, but also for the stronger spatial genetic structure (using the 'Sp' statistic as a measure for quantifying spatial genetic structure, Vekemans & Hardy 2004) Bees and bumblebees are rewarded with copious amounts of nectar, which is secreted at the bottom of the corolla tube. Although floral nectar is believed to be initially sterile, recent investigations have shown that the nectar of P. officinalis is often inhabited by micro-organisms, most often yeasts and bacteria (Jacquemyn et al 2013). Detailed investigations of microbial communities in the floral nectar of ten P. officinalis populations revealed several ascomycote and basidiomycote yeasts, including Metschnikowia reukaufii, Candida bombi, Sporobolomyces roseus and several Cryptococcus species.…”

Section: Floral and Seed Charactersmentioning

confidence: 99%

“…Detailed investigations of microbial communities in the floral nectar of ten P. officinalis populations revealed several ascomycote and basidiomycote yeasts, including Metschnikowia reukaufii, Candida bombi, Sporobolomyces roseus and several Cryptococcus species. Additionally, a large number of bacteria was recovered, which belonged to three major phyla (Actinobacteria, Firmicutes and Proteobacteria) (Jacquemyn et al 2013). The most common bacteria were species from the genera Rhodococcus, Microbacterium and Methylobacterium.…”

Section: Floral and Seed Charactersmentioning

confidence: 99%

“…The most common bacteria were species from the genera Rhodococcus, Microbacterium and Methylobacterium. Other species that were identified (> 97.5% sequence homology with GenBank sequence) included members from the genera Arthrobacter, Bacillus, Brachybacterium, Brevibacterium, Devosia, Erwinia, Enhydrobacter, Flexivirga, Gordonia, Janibacter, Luteipulveratus, Micrococcus, Moraxella, Nocardioides, Okibacterium, Plantibacter, Ponticoccus, Pseudomonas, Rhodanobacter, Saxeibacter, Staphylococcus and Streptomyces (Jacquemyn et al 2013). Although two recent studies have shown that the presence of either bacteria or yeasts can have a profound impact on nectar chemistry and on pollination success and seed set (Herrera, Pozo & Medrano 2013;Vannette, Gauthier & Fukami 2013), the significance of the observed microbes for P. officinalis and its pollination needs to be investigated in more detail.…”

Section: Floral and Seed Charactersmentioning

confidence: 99%

“…Gene flow appeared to occur primarily between adjacent populations, leading to high genetic differentiation in fragmented landscapes and a significant pattern of isolation by distance, whereas in strongly connected landscapes, no isolation by distance was observed. Additionally, Jacquemyn et al (2013) showed that fragmented populations of P. officinalis contained specific communities of nectar-inhabiting micro-organisms that showed low similarity, indicating that foraging by pollinators between populations is limited. These results show that P. officinalis may be susceptible to the deleterious effects of habitat fragmentation and that the long-term conservation of this species calls for specific actions that maintain population sizes, for example by regular opening of the canopy and increasing gene flow between populations.…”

Section: Conservationmentioning

confidence: 99%

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Biological Flora of the British Isles: Pulmonaria officinalis

et al. 2013

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Summary1. This account presents information on all aspects of the biology of Pulmonaria officinalis L. (Common Lungwort) that are relevant to understanding its ecological characteristics and behaviour. The main topics are presented within the framework of the Biological Flora of the British Isles: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, floral and seed characteristics, herbivores and disease, history and conservation. 2. Pulmonaria officinalis is a distylous, perennial rosette hemicryptophyte that is naturalized in Britain. It occurs predominantly in the understory of broadleaved, mixed, open woods rich in hornbeam, beech and oak, but is has also been recorded from hedges, banks alongside streams, (sunken) roadsides, built-up areas, gardens, rubbish tips, yew woodland and, less frequently, coniferous woodland. Its native range stretches from southern Sweden, in the north, to northern Italy, in the south, and from western Germany to Poland and Lithuania. It is most common in central Europe. 3. Pulmonaria officinalis reproduces both by sexual and vegetative means. The underground parts consist of a slowly creeping rhizome with adventitious roots. Despite the presence of an elaiosome that is attractive to ants that likely facilitates seed dispersal, populations often show a significant fine-scale spatial genetic structure and small neighbourhood sizes. 4. The leaves and flowering stalks are covered in hairs of varied length and stiffness, and stems and inflorescences are sparsely covered with glandular hairs. Flowers of P. officinalis are heterostylous, with distinct pin and thrum morphs. The corolla varies from purple, violet or blue to shades of pink and red, or sometimes white. The flowers are mainly pollinated by solitary bees and bumblebees. 5. Pulmonaria officinalis has significantly expanded its distribution in the British Isles since the 18th century, especially in southern England. P. officinalis is currently not regarded as threatened in Europe. Nonetheless, small, isolated populations of the species often show reduced reproductive success and lower genetic diversity, potentially affecting their long-term survival. Preservation of local habitat conditions by regular opening of the forest canopy and restoration of gene flow among populations are required to maintain viable populations of P. officinalis in the long term.

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Endosphere and Endophyte Communities

2023

Microbiomics and Sustainable Crop Production

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Among-Population Variation in Microbial Community Structure in the Floral Nectar of the Bee-Pollinated Forest Herb Pulmonaria officinalis L

Cited by 57 publications

References 42 publications

Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes

Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes

Biological Flora of the British Isles: Pulmonaria officinalis

Endosphere and Endophyte Communities

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