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Probiotics or faecal transplants?

Dave Black


A honey bee nest and its enclosure provides a rich and stable range of ecosystems where we might expect an abundance of microbe populations to thrive, constantly replenished through its interface with the phyllosphere that surrounds it. We know a great deal about the harmful micro-organisms that cause disease; foulbrood bacteria, chalkbrood and nosema, even virus infections, but very little about beneficial micro-organisms that maintain health. Despite a contemporary obsession with prophylactic ‘probiotics’ and gut health there is actually not much known about the contribution from microbes to honeybee fitness, and still less about what the effects of antibiotics and fungicides from pollutants or veterinary treatments might be on the microbiotic environment ‘bees share.


There are two ‘communities’ of bacteria here that are particularly interesting, that associated with the pollen collected and stored for food, and that inhabiting the ‘bee gut itself. Pollen provides the bulk of proteins, vitamins and lipids for colony growth. It is also a warm, moist and sugar rich source of food, albeit acidic, and arrives with its own collection of microorganisms, some well able to exploit it for their own purpose. While it has always been believed pollen stored as ‘bee-bread’ is a pre-digested store of food (similar to honey) closer study show this is probably not true. We find ‘bees prefer pollen less than three days old, that is, they weren’t waiting for some process (akin to fermentation) to occur before eating it. In addition the bacteria counts from collected pollen were low and declined rather than increased. That’s not what we’d expect if the store was supporting the microbes. The populations were so low that it was implausible there were enough to have any effect; the estimate was one microbe for every 2,500 pollen grains. Using microscopy the mostly intact grains did not appear to have been altered in any way by storage, and the bacteria found did not have the characteristics of a stable microbiome but were adapted for survival in acidic, antimicrobial environments. The bacteria in stored pollen are very different from those in the hind gut where pollen is being digested, and where they are present in hundreds or thousands per grain of pollen. It appears then that stored pollen is in a state for preservation rather than conversion, and that actually the true ‘store’ of nutrients is the ‘bees themselves.


We often talk about pollen (fresh or stored) being digested in a ‘communal stomach’. What we mean is that pollen is eaten by a fairly limited group of young bees and fed to everyone else in the colony. These ‘nurse’ bees consume pollen and from glands in their head then secrete a semi-liquid food, This can be pooled in honeycomb cells to feed larvae or shared directly, ‘mouth to mouth’, with the queen and other members of the colony. As nurse bees age and become guard or forager bees they gradually lose the ability to digest pollen and have to be fed by a new generation of nurses. How these ‘bees extract nutrients from pollen grains is not fully understood, but it’s possible microbes play their part. Scanning electron microscope observations of pollen passing through the digestive tract show a range of states, depending on far along the gut you look and, presumably, on the type of pollen grain and its construction. Some are fully ruptured, perhaps because of osmotic shock, others seem more or less intact but empty, the contents removed gradually through the germination pores in the grain.


Another interesting line of research has considered the inevitability of bees consuming the yeasts, bacteria, and fungi that naturally associate with pollen (or nectar) and suggest that this would mean bees are actually omnivorous. Using native (solitary) bees and examining isotopes of carbon and nitrogen in the amino acids glutamic acid and phenylalanine that were consumed the research was able to show the bees were assimilating both microbial and plant proteins. In another study they demonstrated a decline in biomass and increased development time in larvae fed a diet progressively increasing in sterilised pollen, indicating the microbes were an essential part of the diet. This is analogous to leaf-cutter ants growing and consuming fungi grown on the leaf substrate they collect, rather than eating the leaves.


We talk about the bee ‘gut’ as though it was all one homogenous organ, but in reality it is a series of blended zones or organs each with distinct functions and correspondingly different environments and inhabitants. Looking at the microbes in these ‘zones’ is tricky. Older methods rely on culturing bacteria on a growth media, but it possible to miss or underestimate microbes that are unexpected or difficult to culture. Later methods use PCR amplification and genetic makers, but that too has some limitations so that at the moment the most accurate information comes from studies that use and compare both methods, what’s called culture-dependent and culture-independent methods. Working out where these microbes belong is also tricky, some, not adapted to live in a particular environment, may just be passing though and do not form the stable biofilms bacteria flourish in.


Newly emerged ‘bees have no, or only a couple of types, of gut bacteria. ‘Bees acquire bacteria that inhabit their gut from their foraging environment, but also from each other when food is shared. Plainly bacteria in the phyllosphere are present, mostly in the crop, but this is an inhospitable temporary haunt because its contents change so often. It seems unlikely there is a permanent ‘core’ group of bacteria associated with this region, and little evidence for one. The mid-gut and hind-gut do have lasting ‘core’ groups of bacteria and the highest bacterial counts are found here, with most actively growing and reproducing biofilms in the hind gut. The communities have quite different inhabitants from those found in pollen, ‘beebread’ or honey and remain consistent across seasons and geographical regions. When we look closely enough we find that although a gene sequence can indicate a close physiological relationship to other organisms, when it comes to bacteria even closely related species can display remarkable differences in their functional genes. Perhaps surprisingly this simple set of perhaps eight or so core bacteria types are found only amongst eusocial bees, and appear to have diversified to occupy particular niches and perform functions that only apply in groups of honeybees or bumblebees, and that are conserved by their sociality. Long-standing co-evolution has produced functionally unique strains adapted to a symbiotic existence with each other and their bee family, possibly unique even at colony level.


L. M. Klungness, Ying-Shin Peng, Scanning electron microscope observations of pollen food bolus in the alimentary canal of honeybees (Apis mellifera L.) Canadian Journal of Zoology, 1984, Vol. 62, No. 7 : pp. 1316-1319 https://doi.org/10.1139/z84-189


Anderson KE, Sheehan TH, Mott BM, Maes P, Snyder L, et al. (2013) Microbial Ecology of the Hive and Pollination Landscape: Bacterial Associates from Floral Nectar, the Alimentary Tract and Stored Food of Honey Bees (Apis mellifera). PLoS ONE 8(12): e83125. doi:10.1371/journal.pone.0083125


Anderson KE, Carroll MJ, Sheehan T, Mott BM, Maes P, Corby-Harris V. 2014 Hive-stored pollen of honey bees: many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol. Ecol. 23, 5904–5917. (doi:10.1111/mec.12966)


Steffan S, Dharampal P, Danforth B, Gaines-Day H, Takizawa Y, Chikaraishi Y. (2019) Omnivory in bees: elevated trophic positions among all major bee families. Am. Nat.vol. 194, no. 3. doi:10.1086/704281


Dharampal PS, Carlson C, Currie CR, Steffan SA. 2019 Pollen-borne microbes shape bee fitness. Proc. R. Soc. B 286: 20182894. http://dx.doi.org/10.1098/rspb.2018.2894


Philipp Engel, Vincent G. Martinson, and Nancy A. Moran Functional diversity within the simple gut microbiota of the honey bee. 11002–11007  PNAS July 3, 2012 vol. 109 no. 27. https://www.pnas.org/content/109/27/11002


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