Bacterial Species Associated with Highly Allergenic Plant Pollen Yield a High Level of Endotoxins and Induce Chemokine and Cytokine Release from Human A549 Cells

Abstract

Sensitization to pollen allergens has been increasing in Europe every year. Most studies in this field are related to climate change, phenology, allergens associated with different pollens, and allergic disorders. As a plant microhabitat, pollen is colonized by diverse microorganisms, including endotoxin-producing bacteria which may contribute to pollen allergy (pollinosis). Therefore, bacteria isolated from high allergenic and low allergenic plant pollen, as well as the pollen itself with all microbial inhabitants, were used to assess the effect of the pollen by measuring the endotoxins lipopolysaccharides (LPS) and lipoteichoic acid (LTA) concentrations and their effect on chemokine and cytokine release from transwell cultured epithelial A549 cells as a model of epithelial lung barrier. High allergenic pollen showed a significantly higher level of bacterial endotoxins; interestingly, the endotoxin level found in the bacterial isolates from high allergenic pollen was significantly higher compared to that of bacteria from low allergenic pollen. Moreover, bacterial LPS concentrations across different pollen species positively correlated with the LPS concentration across their corresponding bacterial isolates. Selected bacterial isolates from hazel pollen (HA5, HA13, and HA7) co-cultured with A549 cells induced a potent concentration-dependent release of the chemokine interleukin-8 and monocyte chemotactic protein-1 as well as the cytokine TNF-alpha and interleukin-2 to both apical and basal compartments of the transwell model. This study clearly shows the role of bacteria and bacterial endotoxins in the pollen allergy as well as seasonal allergic rhinitis.

Robbsia betulipollinis sp. nov., Isolated from Pollen of Birch (Betula pendula)

“…This possible higher allergic potential is caused by a high lipopolysaccharide concentration (LPS) concentration of the bacteria on the pollen. Interestingly, strain Bol-Pol-6 T has one of the highest measured LPS concentrations in this study with an LPS concentration of 76.6 ng l −1 [ 47 ] and five next relative uncultured bacteria (pairwise similarity values 98.72–99.70%) found in floor dust (FM872738) [ 48 ] and on human skin (HM270658, HM270467, JF167742, JF152894) [ 49 ] are also associated to allergic reaction in these studies.…”

“…Compared to insect-pollinated pollen species (autumn crocus and rape), birch pollen possesses significantly higher species richness and different communities [ 15 ]. Furthermore, it was shown that bacteria and pollen from wind pollinated plants like birch could have a higher allergic potential [ 47 ]. This possible higher allergic potential is caused by a high lipopolysaccharide concentration (LPS) concentration of the bacteria on the pollen.…”

Common Pollen Modulate Immune Responses against Viral-Like Challenges in Airway Coculture Model

“…Also, other factors than endogenous properties of pollen may contribute to their immunomodulatory potency. For example, pollen may contain microbial components [ 31 – 33 ]. In the study by Obersteiner et al [ 31 ], allergenicity of birch was correlated with the high bacterial diversity on pollen.…”

“…In the study by Obersteiner et al [ 31 ], allergenicity of birch was correlated with the high bacterial diversity on pollen. Manirajan et al [ 33 ] noticed that high allergenic plant pollen (e.g., birch) had a higher amount of endotoxins compared to low allergenic plant pollen. Endotoxins, also called as LPS, are the component of the outer membrane of Gram-negative bacteria and recognized by TLR4 on innate immune cells.…”

Is the plant microbiome transmitted from pollen to seeds?

“…Another aspect that began to be deeply investigated is the involvement of pollen-associated microbes in medical issues, more specifically their potential role in the sensitization to the widespread pollen-originating allergic rhinitis (Obersteiner et al, 2016 ; Ambika Manirajan et al, 2022 ) or the effect of propolis used in traditional medicine. On the contrary, the possible implications of pollen as one source of seed microbiome have so far been largely neglected, i.e., the pollen–microbe–seed system has not been investigated yet, as have the microbiomes of other plant habitats (such as the rhizosphere and phyllosphere).…”