Bacterial communities in floral nectar.
TL;DR: It is demonstrated that nectar microbial community are distinct for each of the plant species while there are no significant differences between nectar bacterial communities within nectars taken from different plants of the same species.
Abstract: Summary
Floral nectar is regarded as the most important reward available to animal-pollinated plants to attract pollinators. Despite the vast amount of publications on nectar properties, the role of nectar as a natural bacterial habitat is yet unexplored. To gain a better understanding of bacterial communities inhabiting floral nectar, culture-dependent and -independent (454-pyrosequencing) methods were used. Our findings demonstrate that bacterial communities in nectar are abundant and diverse. Using culture-dependent method we showed that bacterial communities of nectar displayed significant variation among three plant species: Amygdalus communis, Citrus paradisi and Nicotiana glauca. The dominant class in the nectar bacterial communities was Gammaproteobacteria. About half of the isolates were novel species (< 97% similarities of the 16S rRNA gene with known species). Using 454-pyrosequencing we demonstrated that nectar microbial community are distinct for each of the plant species while there are no significant differences between nectar microbial communities within nectars taken from different plants of the same species. Primary selection of the nectar bacteria is unclear; it may be affected by variations in the chemical composition of the nectar in each plant. The role of the rich and diverse nectar microflora in the attraction–repulsion relationships between the plant and its nectar consumers has yet to be explored.
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TL;DR: A broad synthesis of the ecological and agricultural literature focused on seed-microbe interactions as a means of better understanding how these interactions may ultimately influence plant ecology, health, and productivity in both natural and agricultural systems is presented.
Abstract: The development and dispersal of seeds as well as their transition to seedlings represent perhaps the most critical stages of a plant’s life cycle The endophytic and epiphytic microbial interactions that take place in, on, and around seeds during these stages of the plant’s life cycle may have profound impacts on plant ecology, health, and productivity While our understanding of the seed microbiota has lagged far behind that of the rhizosphere and phyllosphere, many advances are now being made This review explores the microbial associations with seeds through various stages of the plant life cycle, beginning with the earliest stages of seed development on the parent plant and continuing through the development and establishment of seedlings in soil This review represents a broad synthesis of the ecological and agricultural literature focused on seed-microbe interactions as a means of better understanding how these interactions may ultimately influence plant ecology, health, and productivity in both natural and agricultural systems Our current understanding of seed-microbe associations will be discussed, with an emphasis on recent findings that specifically highlight the emerging contemporary understanding of how seed-microbe associations may ultimately impact plant health and productivity The diversity and dynamics of seed microbiomes represent the culmination of complex interactions with microbes throughout the plant life cycle The richness and dynamics of seed microbiomes is revealing exciting new opportunities for research into plant-microbe interactions Often neglected in plant microbiome studies, the renaissance of inquiry into seed microbiomes is offering exciting new insights into how the diversity and dynamics of the seed microbiome with plant and soil microbiomes as well as the microbiomes of dispersers and pollinators It is clear that the interactions taking place in and around seeds indeed have significant impacts on plant health and productivity in both agricultural and natural ecosystems
261 citations
Cites background from "Bacterial communities in floral nec..."
...For example, species of Pseudomonas and Bacillus are particularly prevalent in cucurbit fruits, especially within the seed cavity (Fürnkranz et al. 2012; Glassner et al. 2015)....
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...In a study to explicitly examine the nature of the epiphytic bacterial and fungal communities associated with several Triticum and Brassica species, Links et al. (Links et al. 2014) observed that species within each plant genus harbored unique endophytic bacterial communities, which, as in previous studies, were dominated by members of the Proteobacteria (e.g., species of Pantoea, Pseudomonas, Massilia, Xanthomonas, and Telluria)....
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...Compant et al. (Compant et al. 2011) demonstrated that several Pseudomonas and Bacillus species present in flowers resided inside epidermal cells and inside the xylem vessels of ovaries....
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...However, the actual microbial species composition may vary dramatically from one plant species to the next (AizenbergGershtein et al. 2013; Fridman et al. 2012; Jacquemyn et al. 2013) and across geography (Samuni-Blank et al. 2014), both of which may be related, in part, to the strong priority…...
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...Additionally, the morphology of most flowers serves as a protective environment for the developing seed, which concomitantly serves as a protected microbial habitat rich in carbon and nitrogen compounds for microbial growth (AlvarezPerez et al. 2012; Fridman et al. 2012)....
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10 Nov 2017
TL;DR: An overview of the transmission routes that bacteria can take to colonize plants, including vertically via seeds and pollen, and horizontally via soil, atmosphere, and insects is provided.
Abstract: Plants are hosts to complex communities of endophytic bacteria that colonize the interior of both below- and aboveground tissues. Bacteria living inside plant tissues as endophytes can be horizontally acquired from the environment with each new generation, or vertically transmitted from generation to generation via seed. A better understanding of bacterial endophyte transmission routes and modes will benefit studies of plant–endophyte interactions in both agricultural and natural ecosystems. In this review, we provide an overview of the transmission routes that bacteria can take to colonize plants, including vertically via seeds and pollen, and horizontally via soil, atmosphere, and insects. We discuss both well-documented and understudied transmission routes, and identify gaps in our knowledge on how bacteria reach the inside of plants. Where little knowledge is available on endophytes, we draw from studies on bacterial plant pathogens to discuss potential transmission routes. Colonization of roots from soil is the best studied transmission route, and probably the most important, although more studies of transmission to aerial parts and stomatal colonization are needed, as are studies that conclusively confirm vertical transfer. While vertical transfer of bacterial endophytes likely occurs, obligate and strictly vertically transferred symbioses with bacteria are probably unusual in plants. Instead, plants appear to benefit from the ability to respond to a changing environment by acquiring its endophytic microbiome anew with each generation, and over the lifetime of individuals.
239 citations
TL;DR: The purpose of this mini-review is to provide an overview of current knowledge on the diversity, structure and role of the seed microbiota.
231 citations
Cites background from "Bacterial communities in floral nec..."
...habitat Since some micro-organisms can be transmitted by the floral pathway, an overlap in taxa associated with floral structures and seeds has been reported in several plants, including rice [54], grapevine [55], pumpkin [14], apple tree [56 ], Metrosideros polymorpha [57] almond, grapefruit and tree tobacco [58]....
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TL;DR: The crop microbial environment is influenced by worker task, and may function in both decontamination and inoculation, concluding that the crop taxa at low abundance include core hindgut bacteria in transit to their primary niche, and potential pathogens or food spoilage organisms seemingly vectored from the pollination environment.
Abstract: The honey bee is a key pollinator species in decline worldwide. As part of a commercial operation, bee colonies are exposed to a variety of agricultural ecosystems throughout the year and a multitude of environmental variables that may affect the microbial balance of individuals and the hive. While many recent studies support the idea of a core microbiota in guts of younger in-hive bees, it is unknown whether this core is present in forager bees or the pollen they carry back to the hive. Additionally, several studies hypothesize that the foregut (crop), a key interface between the pollination environment and hive food stores, contains a set of 13 lactic acid bacteria (LAB) that inoculate collected pollen and act in synergy to preserve pollen stores. Here, we used a combination of 454 based 16S rRNA gene sequencing of the microbial communities of forager guts, crops, and corbicular pollen and crop plate counts to show that (1) despite a very different diet, forager guts contain a core microbiota similar to that found in younger bees, (2) corbicular pollen contains a diverse community dominated by hive-specific, environmental or phyllosphere bacteria that are not prevalent in the gut or crop, and (3) the 13 LAB found in culture-based studies are not specific to the crop but are a small subset of midgut or hindgut specific bacteria identified in many recent 454 amplicon-based studies. The crop is dominated by Lactobacillus kunkeei, and Alpha 2.2 (Acetobacteraceae), highly osmotolerant and acid resistant bacteria found in stored pollen and honey. Crop taxa at low abundance include core hindgut bacteria in transit to their primary niche, and potential pathogens or food spoilage organisms seemingly vectored from the pollination environment. We conclude that the crop microbial environment is influenced by worker task, and may function in both decontamination and inoculation.
220 citations
Cites background from "Bacterial communities in floral nec..."
...There was considerable variation in the distribution and composition of the microbial communities among libraries, and crops often contained high levels of Enterobacteriaceae (Fig....
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...Corbicular pollen contained a diverse microbiota dominated by non-gut and non-crop bacteria including Actinomycetales, Alphaproteobacteria, Enterobacteriaceae, Pseudomonadales, Firmicutes, and Xanthomonadaceae, (Figs....
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...As an example, the gut of fall individual 1 contained the least amount of the core microbiota, but exhibits a high level of non-core Enterobacteriaceae sequences....
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...Where the core taxa did not dominate the whole gut, the remainder of the library was comprised of sequences belonging to the Enterobacteriaceae, Pseudomonadales, or Alpha 1, a relative of Bartonella spp. identified previously from bees (Fig....
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...Similar to acidic and sugar rich environments of fermented food and silage, the crops of foragers were dominated by Lactobacillus and Alpha 2.2 (Acetobacteraceae), but also contained a small number of sporadically abundant Enterobacteriaceae that likely have their origins in the pollination environment....
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TL;DR: The results reveal that many bacteria prevalent in beebread and the crop are also found in floral nectar, suggesting frequent horizontal transmission, and do not support the core crop bacterial community hypothesized by recent studies.
Abstract: Nearly all eukaryotes are host to beneficial or benign bacteria in their gut lumen, either vertically inherited, or acquired from the environment. While bacteria core to the honey bee gut are becoming evident, the influence of the hive and pollination environment on honey bee microbial health is largely unexplored. Here we compare bacteria from floral nectar in the immediate pollination environment, different segments of the honey bee (Apis mellifera) alimentary tract, and food stored in the hive (honey and packed pollen or “beebread”). We used cultivation and sequencing to explore bacterial communities in all sample types, coupled with culture-independent analysis of beebread. We compare our results from the alimentary tract with both culture-dependent and culture-independent analyses from previous studies. Culturing the foregut (crop), midgut and hindgut with standard media produced many identical or highly similar 16S rDNA sequences found with 16S rDNA clone libraries and next generation sequencing of 16S rDNA amplicons. Despite extensive culturing with identical media, our results do not support the core crop bacterial community hypothesized by recent studies. We cultured a wide variety of bacterial strains from 6 of 7 phylogenetic groups considered core to the honey bee hindgut. Our results reveal that many bacteria prevalent in beebread and the crop are also found in floral nectar, suggesting frequent horizontal transmission. From beebread we uncovered a variety of bacterial phylotypes, including many possible pathogens and food spoilage organisms, and potentially beneficial bacteria including Lactobacillus kunkeei, Acetobacteraceae and many different groups of Actinobacteria. Contributions of these bacteria to colony health may include general hygiene, fungal and pathogen inhibition and beebread preservation. Our results are important for understanding the contribution to pollinator health of both environmentally vectored and core microbiota, and the identification of factors that may affect bacterial detection and transmission, colony food storage and disease susceptibility.
219 citations
Cites result from "Bacterial communities in floral nec..."
...Recent results suggest that floral nectar contains an abundance of unique and diverse bacteria, many of which are highly osmotolerant [101,102]....
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References
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TL;DR: The broad and vague phenotypic definition allowed the genus Pseudomonas to become a dumping ground for incompletely characterized polarly flagellated, gram-negative, rod-shaped, aerobic bacteria, and a large number of species have been accommodated in the genus pseudomonas.
Abstract: The broad and vague phenotypic definition allowed the genus Pseudomonas to become a dumping ground for incompletely characterized polarly flagellated, gram-negative, rod-shaped, aerobic bacteria, and a large number of species have been accommodated in the genus Pseudomonas. The 16S rRNA sequences of 128 valid and invalid Pseudomonas species, which included almost valid species of the genus Pseudomonas listed in the Approved Lists of Bacterial Names, were obtained: sequences of 59 species were determined and those of 69 species were obtained from the GenBank/EMBL/DDBJ databases. These sequences were compared with the sequences of other species of the Proteobacteria. Fifty-seven valid or invalid species including Pseudomonas aeruginosa (type species of the genus Pseudomonas Migula 1894) belonged to the genus Pseudomonas (sensu stricto). Seven subclusters were formed in the cluster of the genus Pseudomonas (sensu stricto), and the resulting clusters conformed well to the rRNA-DNA hybridization study by Palleroni (1984). The other species did not belong to the genus Pseudomonas (sensu stricto) and were related to other genera, which were placed in four subclasses of the Proteobacteria (alpha, beta, gamma and gamma-beta subclasses). Twenty-six examined species, which were not included in the cluster of the Pseudomonas (sensu stricto) and have not been transferred to other genera as yet, are listed alphabetically: 'Pseudomonas abikonensis', Pseudomonas antimicrobica, Pseudomonas beijerinckii, Pseudomonas beteli, Pseudomonas boreopolis, 'Pseudomonas butanovora', Pseudomonas carboxydohydrogena, Pseudomonas cissicola, Pseudomonas doudoroffii, Pseudomonas echinoides, Pseudomonas elongata, Pseudomonas flectens, Pseudomonas geniculata, Pseudomonas halophila, Pseudomonas hibiscicola, Pseudomonas huttiensis, Pseudomonas iners, Pseudomonas lanceolata, Pseudomonas lemoignei, Pseudomonas mephitica, Pseudomonas pictorum, Pseudomonas saccharophila, Pseudomonas spinosa, Pseudomonas stanier, Pseudomonas syzygii and Pseudomonas woodsii. The phylogenetic affiliations of these 26 pseudomonads species are shown.
860 citations
TL;DR: Experimental approaches are necessary to understand the role of toxic nectar in plant-animal interactions, including encouraging specialist pollinators, deterring nectar robbers, preventing microbial degradation of nectar, and altering pollinator behavior.
Abstract: Although plant-herbivore and plant-pollinator interactions have traditionally been studied separately, many traits are simultaneously under selection by both herbivores and pollinators. For example, secondary compounds commonly associated with herbivore defense have been found in the nectar of many plant species, and many plants produce nectar that is toxic or repellent to some floral visitors. Although secondary compounds in nectar and toxic nectar are geographically and phylogenetically widespread, their ecological significance is poorly understood. Several hypotheses have been proposed for the possible functions of toxic nectar, including encouraging specialist pollinators, deterring nectar robbers, preventing microbial degradation of nectar, and altering pollinator behavior. All of these hypotheses rest on the assumption that the benefits of toxic nectar must outweigh possible costs; however, to date no study has demonstrated that toxic nectar provides fitness benefits for any plant. Therefore, in addition to these adaptive hypotheses, we should also consider the hypothesis that toxic nectar provides no benefits or is tolerably detrimental to plants, and occurs due to previous selection pressures or pleiotropic constraints. For example, secondary compounds may be transported into nectar as a consequence of their presence in phloem, rather than due to direct selection for toxic nectar. Experimental approaches are necessary to understand the role of toxic nectar in plant-animal interactions.
496 citations
TL;DR: Monitoring the dominant psychrotrophic species responsible for the production of heat-stable proteolytic and lipolytic enzymes offers a sensitive and efficient tool for maintaining better milk quality in the milk industry.
Abstract: During cold storage after milk collection, psychrotrophic bacterial populations dominate the microflora, and their extracellular enzymes, mainly proteases and lipases, contribute to the spoilage of dairy products. The diversity, dynamics, and enzymatic traits of culturable psychrotrophs in raw milk from four farms were investigated over a 10-month period. About 20% of the isolates were found to be novel species, indicating that there is still much to be learned about culturable psychrotrophs in raw milk. The psychrotrophic isolates were identified and classified in seven classes. Three classes were predominant, with high species richness (18 to 21 species per class) in different seasons of the year: Gammaproteobacteria in spring and winter, Bacilli in summer, and Actinobacteria in autumn. The four minor classes were Alphaproteobacteria, Betaproteobacteria, Flavobacteria, and Sphingobacteria. The dominant classes were found in all four dairies, although every dairy had its own unique "bacterial profile." Most but not all bacterial isolates had either lipolytic or both lipolytic and proteolytic activities. Only a few isolates showed proteolytic activity alone. The dominant genera, Pseudomonas and Acinetobacter (Gammaproteobacteria), showed mainly lipolytic activity, Microbacterium (Actinobacteria) was highly lipolytic and proteolytic, and the lactic acid bacteria (Lactococcus and Leuconostoc) displayed very minor enzymatic ability. Hence, the composition of psychrotrophic bacterial flora in raw milk has an important role in the determination of milk quality. Monitoring the dominant psychrotrophic species responsible for the production of heat-stable proteolytic and lipolytic enzymes offers a sensitive and efficient tool for maintaining better milk quality in the milk industry.
283 citations
TL;DR: The data show that bees which are confronted with plant allelochemicals in nectar and pollen, are not especially adapted (i.e. insensitive) to the plants' defence chemistry.
Abstract: The influence of 63 dietary allelochemicals (alkaloids, terpenes, glycosides,etc.) on the feeding behaviour of bees (Apis mellifera) was tested in terms of deterrency and attraction. For 39 compounds a deterrent (mostly alkaloids, coumarins and saponins) and for 3 compounds an attractive response (mostly terpenes) was obtained in choice tests, which allowed the calculation of respective ED50-values. Under no-choice conditions, 17 out of 29 allelochemicals caused mortality at concentrations between 0.003 and 0.6%. Especially toxic were alkaloids, saponins, cardiac glycosides and cyanogenic glycosides. These data show that bees which are confronted with plant allelochemicals in nectar and pollen, are not especially adapted (i.e. insensitive) to the plants' defence chemistry. GLC and GLS-MS data are given on the alkaloid composition of nectar and pollen ofBrugmansia aurea, Atropa belladonna andLupinus polyphyllus.
264 citations
TL;DR: The results provide compelling evidence that nectar microbial communities can have detrimental effects on plants and/or pollinators via extensive nectar degradation and also call for a more careful interpretation of nectar traits in the future, if uncontrolled for yeasts.
Abstract: The ecology of nectarivorous microbial communities remains virtually unknown, which precludes elucidating whether these organisms play some role in plant-pollinator mutualisms beyond minor commensalism. We simultaneously assessed microbial abundance and nectar composition at the individual nectary level in flowers of three southern Spanish bumble bee-pollinated plants (Helleborus foetidus, Aquilegia vulgaris, and Aquilegia pyrenaica cazorlensis). Yeasts were frequent and abundant in nectar of all species, and variation in yeast density was correlated with drastic changes in nectar sugar concentration and composition. Yeast communities built up in nectar from early to late floral stages, at which time all nectaries contained yeasts, often at densities between 10(4) and 10(5) cells/mm3. Total sugar concentration and percentage sucrose declined, and percentage fructose increased, with increasing density of yeast cells in nectar. Among-nectary variation in microbial density accounted for 65% (H. foetidus and A. vulgaris) and 35% (A. p. cazorlensis) of intraspecific variance in nectar sugar composition, and 60% (H. foetidus) and 38% (A. vulgaris) of variance in nectar concentration. Our results provide compelling evidence that nectar microbial communities can have detrimental effects on plants and/or pollinators via extensive nectar degradation and also call for a more careful interpretation of nectar traits in the future, if uncontrolled for yeasts.
216 citations