The phyllosphere is the community of microbes which live in and on a plant’s leaves. I had no idea that this even existed before writing the section for this website about the microbiome. Of course, if you think about it for a microsecond, it must! Our world has more microbes than anything else by several orders of magnitude, so, there must be microbes in a tree’s leaves. But the phyllosphere has been less publicised due to the intense interest in the rhizosphere (root microbiome) and in its beneficial microbes which can help plants grow by manipulating the soil and root environment.
The phyllosphere is different to the rhizosphere in that its main microbial members are bacteria and not fungi, although fungi are present, along with some archaea. It has been estimated that there are 1 million -10 million bacterial cells per cm2 of leaf surface.ref And worldwide, the phyllosphere is an important microbiome, with a possible 1026 cells! But it’s a relatively hostile environment, with fluctuating temperature & humidity and limited nutrients on the leaf surface. The shape and structure of the leaf at a microscopic level provides a range of microhabitats for bacteria, including the bases of trichomes, stomata, hydathodes (leaf pores), grooves along the veins, epidermal cell junctions, and cuticle depressions.ref A study into tree phyllospheres found 129 bacterial species were significantly associated with the gymnosperms including Armatimonadetes, Actinobacteria, Bacteroidetes, Acidobacteria, TM7, TM6, Deltaproteobacteria, OD1, Fusobacteria, and FBP and 79 with the angiosperms including Chlamydiae, Proteobacteria, Gammaproteobacteria, Alphaproteobacteria, and Firmicutes.ref
What determines the microbial mass and mix on leaves is a combination of different factors, including the nitrogen content of leaves, the specific leaf area (related to carbon availability), wood density and seed massref and the largest part of the variation seen between phyllospheres comes down to the host species. Conifers have a different phyllobiome than other species, for example they have less ice nuclei active bacteria (bacteria which can cause ice crystals to form) and they have Frankiaceae which is involved in nitrogen fixing in the soil.ref Location also plays a role, with urban trees displaying a different phyllosphere makeup – correlated to ultrafine particulate matter and black carbon on the leaves.ref
Bacteria usually require an available carbon source. You might be surprised to know that similar to roots, leaves also produce exudates (substances they exude into the environment). These include a wide range of carbon compounds, such as carbohydrates, amino acids, organic acids, and sugar alcohols, primarily products of photosynthesis, as well as proteins, oils, secondary metabolites and mucilage.ref These carbon sources are not the only ones – the Methylobacterium species can use methanol exuded from the leaf from the breakdown of pectin as its only carbon source.ref One of the bacterial families found on birch – Rhodospirillaceae – is able to photosynthesise, removing the dependence on leaf carbon sources. Another study discovered that certain phyllosphere bacteria can use diesel for their carbon source!ref
Similarly, bacteria in the rhizosphere produce a range of substances just like they do in the rhizosphere – biosurfactants which reduce surface tension, degrade hydrocarbons and improve moisture levels and dissolved nutrients on the leaf surface, plant growth regulators which open up the leaf cells and cause them to leak nutrients, enzymes which help break down nutrients and protect the bacteria from solar radiation, and phytotoxins (if the bacteria is a pathogen).ref
The benefits of phyllosphere microbes to their host are similar to those in the rhizosphere – for example Acetic Acid Bacteria have been found to perform nitrogen fixation within the needles of Pinus flexilisref, others confer resistance to Bursaphelenchus xylophilus-induced pine wilt diseaseref, some phyllosphere fungi produce zeatin, a cytokinin (plant growth regulator)ref and others auxins, some also produce anti-freeze proteins which lower the freezing temperature on the leaf.ref Bacteria are implicated in the bioremediation of harmful chemicals or pollutantsref, improved tolerance to stress, production of proteins which trigger the plant to mount defences against pathogens as well as those which attract populations of beneficial fungi.ref
So, just like the rhizosphere, the phyllosphere is a very active place with many microorganisms playing different roles and constantly interacting in a dynamic ecosystem. What this means for bonsai is that there likely are organisms in the foliage which benefit your plant. Similar to the advice in general around the microbiome, applying fungicides, anti-bacterials and chemical pesticides can kill phyllosphere organisms so avoiding this is a good idea.