Nectar bacteria stimulate pollen germination and bursting to enhance their fitness

Abstract

For many flower visitors, pollen is the primary source of non-carbon nutrition, but pollen has physical defenses that make it difficult for consumers to access nutrients. Nectar-dwelling microbes are nearly ubiquitous among flowers and can reach high densities, despite the fact that floral nectar is nitrogen limited, containing only very low concentrations of non-carbon nutrients. Pollen contains trace micronutrients and high protein content but is protected by a recalcitrant outer shell. Here, we report that a common genus of nectar-dwelling bacteria, Acinetobacter, exploits pollen nutrition by inducing pollen germination and bursting. We use time course germination assays to quantify the effect of Acinetobacter species on pollen germination and pollen bursting. Inoculation with Acinetobacter species resulted in increased germination rates within 15 minutes, and bursting by 45 minutes, as compared to uninoculated pollen. The pollen germination and bursting phenotype is density-dependent, with lower concentrations of A. pollinis SCC477 resulting in a longer lag time before the spike in germination, which is then closely followed by a spike in bursting. Lastly, A. pollinis grows to nearly twice the density with germinable pollen vs ungerminable pollen, indicating that their ability to induce and exploit germination plays an important role in rapid growth. To our knowledge, this is the first direct test of non-plant biological induction of pollen germination, as well as the first evidence of induced germination as a method of nutrient procurement, as the microbes appear to hijack the pollen’s normally tightly controlled germination mechanisms for their benefit. Our results suggest that further study of microbe-pollen interactions may inform many aspects of pollination ecology, including microbial ecology in flowers, the mechanisms of pollinator nutrient acquisition from pollen, and cues of pollen germination for plant reproduction.

Pollen and yeast change nectar aroma and nutritional content alone and together, but honey bee foraging reflects only the avoidance of yeast

“…This study provides evidence that even when pollen grains remain intact, pollen can provide amino acids to nectar and improve microbial growth. Furthermore, because M. reukaufii inoculation did not result in obvious damage to pollen as has been reported for other nectar microorganisms (Christensen et al, 2021), it may be that this yeast has limited negative impacts on plant reproduction and particularly male fitness, as has been reported previously (Schaeffer and Irwin, 2014;Yang et al, 2019; but see Herrera et al, 2013). Our results also suggest a previously overlooked and important role of pollen in nectar sugar concentrations, decreasing sucrose via its conversion to glucose and fructose.…”

“…Because nectar contains high sugar concentrations and a paucity of amino acids and proteins, pollen has been hypothesized to provide a key source of nitrogen to nectar‐inhabiting microorganisms. Microbes have been observed clustering around and sometimes rupturing pollen grains (Herrera, 2017) and recent studies have confirmed that pollen increases the population density of nectar‐inhabiting microbes (Pozo and Jacquemyn, 2019; Christensen et al ., 2021). Some Acinetobacter species trigger pollen germination, thereby improving access to pollen nutrients (Christensen et al ., 2021).…”

“…Microbes have been observed clustering around and sometimes rupturing pollen grains (Herrera, 2017) and recent studies have confirmed that pollen increases the population density of nectar‐inhabiting microbes (Pozo and Jacquemyn, 2019; Christensen et al ., 2021). Some Acinetobacter species trigger pollen germination, thereby improving access to pollen nutrients (Christensen et al ., 2021). However, chemical analyses which track bioavailable nitrogen within the pollen‐nectar system are still lacking.…”

Are microbes growing on flowers evil? Effects of old flower microbes on fruit set in a wild ginger with one-day flowers, Alpinia japonica (Zingiberaceae)

“…Alternatively, bacteria and/or fungi dominant on old flowers might have indirectly decreased fruit set by changing the microenvironment of flowers. Some flower microbes are known to inhibit pollen germination or pollen tube growth (Christensen et al 2021; Eisikowitch et al 1990), while the effects of microbes on other post-pollination processes are largely understudied (Cullen et al 2021). On the other hand, it is unlikely that pollinator behavioral response affected the fruit set as reported in previous studies (Sobhy et al 2018; Vannette et al 2013), because we hand-pollinated the flowers under the fruit set monitoring.…”

Are microbes growing on flowers evil? Effects of old flower microbes on fruit set in a wild ginger with one-day flowers, Alpinia japonica (Zingiberaceae)

“…Nectar yeasts are reported to modify pollinator foraging patterns and reduce pollination success (Herrera et al 2013). Acinetobacter bacteria that commonly inhabit floral nectar exploit pollen nutrition by inducing pollen germination and bursting (Christensen et al 2021). Most studies of these phenomena examined the effects of an individual microbial species or of separate strains rather than that of the whole community.…”