In the guts of bees

By Nicola Temple

We hear a great deal about the beneficial bacteria that live in our digestive system and commonly referred to as the microbiome, which help us turn indigestible materials into nutrients that we can absorb. There are countless probiotic products on the market that are meant to introduce more of these beneficial bacteria into our system, enriching our microbiome. However, humans and indeed mammals are not alone in having helpful microflora in the gut.

The microbes that inhabit the guts of social bees has been of particular interest recently. These microbial communities have been studied for their role in bee health, but also as a model organism to help understand the relationship between hosts and their gut microbes, potentially providing insight into our own system.

The specialised cast of microbes

The microbiome of bees is relatively simple, but very specialised. There are about eight to ten bacterial species, but different species of bee will carry different strains of these bacterial species. The bacteria are so specialised that a strain from one bee genus isn’t able to colonise the gut of a bee from a different genus. This suggests that these bacterial strains have been evolving with their hosts over a very long period of time.

Nest entrance of the stingless bee, Geniotrigona thoracica, is
from Malaysia. Photo credit: Eunice Soh.

Like us, these bacteria help the bees break down complex molecules through fermentation in order to make the nutrients available to the hosts. There’s also evidence that they might help to neutralise toxins in the gut. These friendly microbes also outcompete nastier pathogenic species that can make the host ill. For example, the gut microbes in bumblebees have been linked to lower levels of the parasite Crithidia bombi.

The gut microbes of non-social insects, including solitary bees, aren’t as specialised because they acquire them from their environment rather than from other members of their species. Among social bees, it is behaviours such as passing food between individuals and feeding larvae, that allow an exchange of microbes. However, these exchanges pass along the bad microbes as well as the good.  Beekeepers are painfully aware that pathogens can pass through a colony like wildfire. Social insects therefore need a very responsive system that helps keep these pathogens in check. And the key to this might be a very ancient relationship between the good microbes and the host bees themselves, which allows the bee’s immune system to quickly identify the less desirable critters.

A long-term relationship

Research published this week in the journal Science Advances suggests that five of the species of gut bacteria found in modern social bees have been evolving along with their hosts for about 80 million years. It was around this time that the first solitary bees began socialising with other bees – sharing nests and food resources and making concerted defence efforts. The descendants of these first social bees are the hundreds of species of honey bees, bumblebees and stingless bees that are alive today.
This finding not only shows that social creatures, such as bees and humans, transfer bacteria among each other during the same lifetime, they pass them along generations, enabling the microbiome and host to evolve together.

“The fact that these bacteria have been with the bees for so long says that they are a key part of the biology of social bees,” says Nancy Moran, a professor of integrative biology at the University of Texas who co-led the research with postdoctoral researcher Waldan Kwong. “And it suggests that disrupting the microbiome, through antibiotics or other kinds of stress, could cause health problems.”
The co-evolution of the gut bacteria and the bees is so closely linked, in fact, that the researchers found that when a new species of bee branches off in the evolutionary tree, a new strain of bacteria branches off with it. The result being that each of the hundreds of species of social bees alive today has its own specialised strains of gut microbes.

Human influence on this long-term relationship

It’s currently unknown how toxins introduced by humans, including pesticides, might affect the bee microbiome. There is recent evidence, however, that the prophylactic use of antibiotics by bee keepers in the US has resulted in some gut bacteria in honeybees developing antibiotic resistance.

References

Engel, P. et al. 2016. The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions. mBio 7 (2): e02164-15.

Kwong, W.K., Medina, L.A., Koch, H., Sing, K-W., Soh, E.J.Y., Ascher, J.S., Jaffe, R. & Moran, N.A. 2017. Dynamic microbiome evolution in social bees. Science Advances 3: e1600513.

Kwong, W.K., Engel, P., Koch, H. & Moran, N.A. 2014. Genomics and host specialization of honey bee and bumble bee gut symbionts. PNAS 111 (31): 11509-14.

A portrait of a boy and his plant

By Nicola Temple

On the 12th of February 1809, Charles Darwin was born in a large Georgian house, known as The Mount, in Shrewsbury. As a biologist, I am very familiar with the works of Darwin. And when I conjure an image of this man in my head it is of him in his 60s, bald on top and with a formidable beard. However, on a recent visit to the University of Bristol Botanic Garden, the curator, Nick Wray, showed me a portrait I had never seen before.

The portrait was completed in 1816, just before Darwin turned 7 years old and he is with his sister Catherine. It is a magnificent piece done using chalk on paper, by the artist Ellen Wallace Sharples (1769-1849), who was settled in Bristol at the time – not far from the Botanic Garden in Clifton [see note 1].

Nick pointed the portrait out to me because he is interested in the plant that Darwin is holding in the portrait. Children would have often been given something to hold while sitting for a portrait – it gave them something to do with their hands to prevent fidgeting. While Catherine has a posy of flowers in her hand, Charles is holding a clay pan on his knee with a plant in full bloom. This would have been no small feat for a child.

The portrait painted by Ellen Wallace Sharples in 1816
of Charles and Catherine Darwin.

Nick recognised the plant held by Darwin as almost certainly Lachenalia aloides (the opal flower), which is a native to the Western Cape of South Africa. Nick informed me that Cape flora were very in vogue during this period. The collecting activities and botanical observations of horticulturist-explorers, such as W. Paterson, Francis Masson, Robert Gordon, W.H.C. Lichtenstein, John Barrow and William Burchell, created a voracious appetite among Europeans for the curious plants of the Western Cape, while established trade routes enabled their transport back to Europe. So it is very likely that the children of a wealthy family would have been given such exotic pieces to hold rather than a favourite toy.

The artist almost certainly painted the portrait at the Darwin’s family home, The Mount. Records show that their impressive house had equally impressive gardens, including a conservatory and hothouse. The Lachenalia aloides likely came from one of their own glasshouses. Grown correctly in a cool frost free glasshouse, this little plant flowers from February-March. In a warm glasshouse it would flower earlier.

In an article written for the Garden History Society by Susan Campbell (Vol. 40, No 2 Winter 2012), she lists the plants cultivated at the Mount, including those growing in the Conservatory and Hothouse. In these lists, one species of Lachenalia is mentioned, Lachenalia pendula, which is now known as Lachenalia bulbifera. This species is almost always red in colour with the robust flower spike leaning to one side. However, yellow tipped orange forms have been recorded in the wild. Whether the plant in the portrait was misidentified in the original plant list or it was correct and an unusual orange and yellow form was cultivated, we shall never know. On examining the portrait carefully, its habit, erect inflorescence and the colour of the flowers, suggests the plant was wrongly identified and should be Lachenalia aloides. Nick goes onto suggest that, “the presence of this Cape bulb flowering in this portrait is evidence that the chalk picture was made around the 12 February 1816, Charles Darwin’s seventh birthday. The picture may have been commissioned deliberately to commemorate the occasion”.

About Lachenalia aloides

There are about 110 different species of Lachenalia, 80 of which are found in the Cape region of South Africa. L. aloides has a number of different varieties, all of which grow on granite or sandstone outcrops. The flowers can vary quite a bit in their colour. Some plants have flowers that are nearly entirely yellow, while others are magenta at the base turning yellow and then to green.

The Lachenalia genus are geophytes, which means that they spend part of the year dormant as a fleshy underground structure, such as a bulb, rhizome or tuber. South Africa is a global hotspot of geophyte diversity. There are 2,100 species across 20 different families in the area and 84% of them are endemic.

Lachenalia aloides is naturally pollinated by sunbirds, which use their long curved bill to access the nectar at the base of the tubular flowers. It was widely-thought until fairly recently that sunbird-pollinated plants had almost always evolved perch-like structures to make feeding for the sunbird easier. However, L. aloides has no such structure and the sunbirds simply sit on the ground to feed on the flowers – an observation that has been made with other low-growing sunbird-pollinated species.

Lachenalia in the Botanic Garden

Lachenalia aloides is in bloom at the
Botanic Garden right now if you want to
have a look at this interesting South African bulb.

The Botanic Garden has some specimens of Lachenalia aloides and other Lachenalia species in the glasshouses and, much like the plant Darwin is holding in the portrait, they are currently in bloom. The portrait would have been painted around this time of year, when there would have been very few plants in bloom. This further supports Nick’s conclusion regarding the species.

The Lachenalia story was one aspect of a lecture titled The Origin & Diversity of Flowering Plants, which was given recently by Nick Wray to the members of the annual Darwin Festival, held each February in Shrewsbury. The audience, made up of academics, ecologists, naturalists and keen amateur and professional gardeners, were taken through the flower pollination syndromes, illustrating the diversity that has evolved over millions of years. Nick discussed the work of the Angiosperm Phylogeny Group (APG) work, the planting of the APG III displays at the Botanic Garden and the difficult task of cultivating Amborella trichopoda and its place at the base of the extant living Angiosperm phylogenetic tree. The talk was illustrated by plants that were brought from the Botanic Garden. This created a lot of interest and added to the sense of place as the talk was held in the Shrewsbury Unitarian Church where Darwin’s mother took him and her other children to worship until Charles was thirteen. When, with an eye to his future university life, Darwin would have to attend a Church of England Church to ensure he would be eligible for a university course as students from Unitarian families would not be admitted.

The group were very appreciative of Nick’s talk and plan to make a summer visit to the Botanic Garden to enjoy the garden and explore its various evolution displays.

Notes:

1. Ellen Wallace Sharples met her husband in Bath where he was her tutor. After they married, the couple travelled back and forth a couple of times between England and America. When Ellen’s husband died in 1810, she moved to an apartment in Clifton with her two children (also artists) in 1811. She made her living doing portraits, as did her children. When she died in 1849, she left a substantial sum to the Bristol Academy which was instrumental in financing Bristol’s first art gallery, now the Royal West of England Academy.

Sources:

Campbell, S. 2009. ‘Sowed for Mr C.D’: The Darwin family’s garden diary for The Mount, Shrewsbury, 1838-65. Garden 
     History 37 (2): 1-16.
Campbell, S. 2012. ‘Its situation…was equisite in the extreme’: ornamental flowers, shrubs and trees in the Darwin 
     family’s garden at The Mount, Shrewsbury, 1838-65. Garden History 40 (2): 1-32.
Procheş, Ş., Cowling, R.M., Goldblatt, P., Manning, J.C., Snijman, D.A. 2006. An overview of the Cape geophytes. 
     Biological Journal of the Linnean Society 87: 27-43.
Turner, R.C., Midgley, J.J. 2016. Sunbird-pollination in the geoflorous species Hyobanch sanguinea (Orobanchaceae) 
     and Lachenalia luteola (Hyacinthaceae). South African Journal of Botany 102: 186-9.

The evolution of a predatory plant

By Nicola Temple

We keep a Venus flytrap (Dionaea muscipula) in our bathroom. My son begged me for it, which inevitably means I look after it. Having seen these carnivorous little delights in the glasshouses at the University of Bristol Botanic Garden, I have learned that humidity and moisture are key to its happiness – hence it’s bathroom location and its constant immersion in a tray of water.

The leaves of  the Venus flytrap, open (foreground) and
wrapped around its prey (background, right).
Photo credit: Shelby Temple
While I mostly leave my son to do the part he loves best – feeding – I can’t deny my own fascination with it. The leaves, converted to ambush traps through evolution, have to have enough stimulation by an unsuspecting insect to warrant the plant investing the energy to snap the trap shut.  Once the trap is shut, the plant estimates the size of the prey based on the amount of stimulation of the sensory ‘hairs’ triggered by the trapped (and no doubt panicked) insect. If there is a sufficient signal from the sensory hairs, the plant starts to produce enzymes and proteins that will help it digest and absorb the prey. It’s the stuff of nightmares…for the insect.
So what evolutionary steps transformed a leaf designed to harvest light from the sun into a leaf designed to trap prey? New research published this week in the journal Genome Researchhas provided some insight into the origins of the Venus flytrap’s trap.

It’s a leaf with a hint of root and a dash of…tongue?

Professors Rainer Hendrich and Jörg Schultz led a team of scientists from Julius-Maximilians-Universität Wüuzburg (JMU) in Bavaria, Germany who looked at the genes being expressed by the traps. They found that the traps not only had active genes typical of leaves, but also those typically found in roots.
A close up view of the trap, which shows the sensory ‘hairs’.
Photo credit: Shelby Temple
There are dome-shaped glands on the surface of the trap. The outer layer of each gland secretes the digestive enzymes, but the middle layer has foldings that increase the surface area – reminiscent of microvilli in the human intestine. It is thought that this is where nutrient absorption takes place. As this is a major function of roots, it is not surprising that some of the same genes are required.
Now…about about that tongue. I mentioned above that the plant releases digestive enzymes if it receives enough stimulation within the closed trap. But what if the insect dies very quickly after being trapped? The plant has a receptor in the trap that can detect chitin – the main constituent of an insect’s exoskeleton.  So even if the insect is no longer moving, the plant can ‘taste’ the insect in the trap and begin digesting.


Switching from defence to offence

When non-carnivorous plants come into contact with chitin, it is usually not going to turn out well for the plant –  they are under attack by herbivorous insects. Henrich and Schultz looked at the defence mechanism triggered by insects feeding on the non-carnivorous plant thale cress (Arabidopsis thaliana). They found that the plant in defence mode activates the same genes in the same pattern as the Venus flytrap in attack mode.
“In the Venus flytrap these defensive processes have been reprogrammed during evolution. The plant now uses them to eat insects,” explains Hedrich.
In both cases, mechanical stimulation (whether a chewing insect or a trapped one) generates an electrical impulse that activates the release of the hormone jasmonate. In Arabidopsisthis hormone begins a cascade of events that starts the production of various chemicals that deter the insect or make the leaves hard to digest. In the Venus flytrap, however, jasmonate starts the digestion of the insect and uptake of the nutrients.
So, the ancestor of the Venus flytrap had all the machinery in place for detecting insects and triggering a chemical response to their presence, but evolution managed to shift it from a defensive strategy to a very effective offence.

Source: 

“Venus flytrap carnivorous life style builds on herbivore defense strategies”, Felix Bemm, Dirk Becker, Christina Larisch, Ines Kreuzer, Maria Escalante-Perez, Waltraud X. Schulze, Markus Ankenbrand, Anna-Lena Keller Van der Weyer, Elzbieta Krol, Khaled A. Al-Rasheid, Axel Mithöfer, Andreas P. Weber, Jörg Schultz, Rainer Hedrich. Genome Research, DOI: 10.1101/gr.202200.115