A MICROBIAL WORLD MAY CONTROL THE INNER WORKINGS OF WILD ANIMALS
By Kristen J. DeMoranville and Clara Cooper-Mullin, University of Rhode Island
Read more by Kristen and Clara on their blog, Animals Living With Change
WHAT DO WE KNOW ABOUT MICROBES AND ANIMAL PHYSIOLOGY?
Scientists have recently learned about a hidden world of microorganisms, or microbes, that may control a lot of human and animal physiology, or the ways in which our body functions. Microbes promote human health, yet it remains undiscovered how microbes help animals in the wild. This backgrounder highlights scientific understanding of how microbes influence seasonal events in wild animals, such as hibernation and migration, and explains how scientists are tackling this new and exciting frontier.
HOT RESEARCH QUESTIONS
1. IS THERE A REGULAR PATTERN OF HOW THE ANIMAL MICROBIOME CHANGES WITH THE SEASONS? IS THERE A MIGRATORY MICROBIOME?
2. DOES THE MICROBIOME FACILITATE SEASONAL CHANGES IN HOST DIET, PHYSIOLOGY, OR BEHAVIOR? DO MICROBES AID HIBERNATING AND MIGRATING ANIMALS?
3. HOW ARE THE SHIFTING GUT MICROBIOME COMMUNITIES POPULATED? WHAT PROPORTIONS OF MICROBES ARE INHERITED FROM HOST PARENTS? ARE NEW MICROBES INTRODUCED THROUGH DIET AND MATING?
Microbes’ roles on host physiology under shifting environmental conditions
Three areas of study--microbiology, physiology, and ecology--have established that each host animal is home to a hidden ecosystem called the microbiota. Trillions of microbes living within us help us to digest our fibrous foods and prevent common diseases. These little helpers can even be shared with our loved ones through close contact. Most of these discoveries have been described in humans, whose steady routines make for a fairly static suite of internal microbes. However, scientists have discovered that these hidden worlds can change predictably throughout the year as we change our lifestyles. This has been demonstrated in the guts of people who seasonally change their diets or switch up their exercise routines.
Studying the patterns of microbial change in humans is difficult because there aren't many populations that rely exclusively on seasonal foods or are willing to exercise while keeping all other daily activities controlled. Instead, scientists are turning to wild animals to investigate these questions, because animals and their microbes consistently experience fluctuating conditions, such as diet and activity levels, on an annual basis. As in humans, microbes in wild animals aid in the survival of their host through shifting environments by controlling aspects of their physiology.
Understanding this tightly linked microbe-animal host relationship will inform conservationists about the foods that microbes require and therefore how to best manage habitats. It will also enable medical scientists to compare similar relationships in humans in order to understand how microbes lighten symptoms of diseases and identify appropriate diet and exercise regimes to keep human microbes happy and healthy.
How do we study animal microbes?
It's a challenge to study the microbes that reside within the nooks and crannies of our bodies. Scientists have optimized the methods and equipment needed to detect the trillions of microorganisms that live inside each and every animal on our planet by studying an animal’s microbiome.
Sidebar: How to identify the microbes living within you
Microbiota is the collection of microorganisms living within a host, and the microbiome is the collection of their genomes (DNA) or transcriptomes (RNA). Scientists use sequencing techniques–a series of steps to extract and isolate genetic material–to identify the specific DNA and RNA combinations that identify a microorganism. Over the last decade, sequencing techniques have become affordable and time-efficient, enabling scientists to characterize the number and types of microorganisms that make up an animal's microbiome. To get a clearer picture about how the microbiome functions within a host, researchers are beginning to manipulate specific variables, such as diet, and sequence RNA samples to identify the microbes present and determine how they respond.
Research on microbiomes is still largely exploratory
There are likely more complex interactions between the microbes and their animal hosts than we currently recognize. We do know that all animals have mutually dependent relationships with their microbiome.
*Although not all microbes are beneficial to the host
Examining microbes from well-studied animals, like humans and laboratory mice, has taught us how the microbiome functions in animals who live in relatively stable environments. However, most animals live in the wild and regularly experience fluctuating environments as seasons change, as they move throughout their habitat, or as they migrate to new habitats. This means that the conditions within the animal host also shift as the host eats new foods, encounters novel microbes, changes its activity levels, and fluctuates its body temperatures. Wildlife physiologists suspect that the microbiome is just as dynamic as the host.
We know that the microbiome can change dramatically over short time periods mostly from researching animals during their early growth and development phases, and these extreme community changes are demonstrated by the way that we build our microbiome at birth. Newborn babies first acquire starter-pack microbes from their mother's birth canal and from her milk. Every subsequent interaction the baby has introduces novel microbes; hugs and kisses from siblings, pets, and others outside the nuclear family help to establish a diverse microbe community that works to develop the baby's healthy digestive tract and immune system.
THE KNOWN UNKNOWNS
Microbiome research is advancing rapidly, but several big questions face scientists who study microbiomes in wildlife:
1. Is there a regular pattern for how an animal’s microbiome changes with the seasons?
2. Does the microbiome drive seasonal changes in host diet, physiology, or behavior?
Wild animals adjust to their changing environments
As temperatures cool and food resources become scarce in the fall, animals must adjust their behavior and transform their bodies to cope with these extreme annual environmental changes. No animal is experiencing these seasonal changes alone. In fact, they are accompanied by billions to trillions of microorganisms covering every surface on and within their bodies: their microbes. Many mammals, like the ground squirrel, survive harsh winter conditions by ceasing almost all activity to preserve their energy during hibernation. The ground squirrel may fast for up to nine months, living off its stored body fat. To ensure that its fat lasts through hibernation, these mammals minimize the energy they use by reducing their brain synapses, the size of their digestive tract, and their heart rate and metabolism. Hibernators must then reverse these changes to emerge in the spring and be ready to eat a complex diet again.
Other animals, like the Blackpoll Warbler, enact an opposite survival strategy, where they increase their activity to migrate to southern latitudes in search of more abundant food resources. Remarkably, the Blackpoll Warbler flies for up to five days without stopping during migration. These migratory flights burn most or all of the birds’ fuel stores and reduce the size of their digestive organs. Migrating songbirds must stop along their migration to first rebuild their digestive tracts and then take advantage of ripe fruits to quickly pack on body fat to continue their journey. A typical migratory songbird punctuates short, energy-intense flights with these longer periods of resting and refueling at stopover sites, so birds must be able to change their bodies on shorter timescales than hibernators.
The return of spring thaws frozen grounds and provides resources needed for hibernating animals to emerge and songbirds to return to temperate areas. An animal’s microbiome most likely exists along a spectrum of assistance, where it plays an active role in helping its host through these changes, or, less likely, it is merely a passenger along for the ride.
Researchers are just discovering how the microbiome aids mammals during hibernation, or how physical changes to a hibernating animal affects the types and number of microbes that compose the microbiome. Others are studying how a bird’s microbiome aids in processing fats to prepare for migratory flights or how it facilitates switching from an insect diet to a fruit diet during fall migration. See below for a list of scientists doing this work.
Wild microbes adjust to their changing host environments
Just as wild animals experience changes in their environments, the animals provide an equally changing internal environment for their microbes. The microbiome consists of a fluctuating group of specific microbes including bacteria, fungi, viruses, and other single-celled organisms whose presence and abundance responds to host conditions. During ground squirrels’ hibernation, their microbiome is also forced to fast, and the lack of new nutrients causes the different species of microbes to compete for resources. A small number of species are specialized to survive in these low nutrient environments by feeding on mucus linings of the gut, and during hibernation they outcompete the species who make a living by feeding on plant material. This constant competition during hibernation can completely change the microbe community in the gut. Conversely, there's a greater number of microbe species present in the gut of squirrels during the active season, and the microbes that are best at breaking down plant material are the most abundant. Therefore, the physiology of a hibernating, fasting ground squirrel affects the types and number of microbes inhabiting its body, but little is known about how these microbes get to the squirrel’s gut in the first place. Are these microbes inherited from an organism's parents? Do they enter the body through the host's changing diet?
During migration birds also undergo intense metabolic remodeling, meaning they have an enhanced ability to use fat stores during flights and a remarkable ability to rebuild their fat stores during migratory breaks (stopovers). These migratory dynamics change the resources available to their microbiomes; the nutrients available to the microbiome fluctuate wildly from large influxes of fats from fruits eaten on stopovers to fasting during migratory flights. The microbiome in migratory birds is a new avenue of research, so it is not yet known if the gut microbiome communities are as dynamic in birds as they are in hibernators.
Recent studies suggest that microbes are changing across a bird's annual cycle. Swainson’s Thrushes and Gray Catbirds, two common migrants in North America, have gut microbiota composed of very different species during spring migrations versus fall migrations. This shift likely results from the birds’ exposure to different food sources, such as greater availability of fruits than insects during fall versus spring migration. Additionally, actively migrating shorebirds have higher numbers of a particular bacterial genus (Corynebacterium) as compared to non-migrating shorebirds. The cause underlying changes to the microbiome and how these changes affect migrating birds, however, is still a mystery.
WHAT'S NEXT?
Scientists have established that there is a characteristic hibernating microbiome. However, researchers predict that the microbiome of migrating birds remodels itself in the face of extreme changes in host metabolism, host diet, and host habitat. Is there a migratory microbiome, and if so, what does it look like?
Scientists are making huge advances by learning how microbes change in shifting environments, but there are fundamental questions that remain unanswered. How do microbes help to initiate and reverse metabolic changes in hibernators and migrators? Researchers are currently designing experiments to manipulate microbe communities under specific conditions to understand the link between microbes and host physiology. Identifying the microbes critical for helping animals transition through their annual cycles and identifying the specific requirements for those microbes will enable conservationists to manage resources for both microbe and animal survival, especially as global environmental conditions change in response to climate change and habitat loss.
For More Information
Sources
M. Denise Dearing - University of Utah - Dr. Dearing studies how the microbes inhabiting the gut of woodrats help these herbivores to degrade toxins naturally occurring in their diet.
Kathryn M. Docherty - Western Michigan University - Dr. Docherty has investigated how the microbiome can relay genetic information about potential mates in Leach’s storm petrels, and has done work surveying the microbiome on the skin and in the gastrointestinal tract in songbirds.
Sarah Hird - University of Connecticut - Dr. Hird's lab examines how the microbiome varies across bird species, as well as within a species. She aims to examine how a bird’s unique adaptations (flight, feathers, eggs, migration) have shaped their microbiomes during evolutionary history.
Staffan Jacob - Station d’Ecologie Théorique et Expérimentale - Dr. Jacob focuses on the different traits involved in communication, cooperation, dispersal and host-microbes interactions.
Kevin Kohl - University of Pittsburgh - Dr. Kohl's lab focuses on understanding how the microbes within fish, amphibians, reptiles, birds, and mammals influence host physiology, ecology, and evolution. Recent studies have focused on: the microbial ability to detoxify food in wood rats and greater sage grouse, the distinct amphibian microbiomes in tadpole and adult life history stages, the amphibian microbial response to pollutants and temperature.
Jose C. Noguera - University of Vigo - Dr. Noguera has studied how stress hormones (Glucocorticoids) can modulate a bird’s microbiome in its gastrointestinal tract.
Michael Taylor - University of Aukland - Dr. Mike Taylor is characterizing the microbiomes of endangered species (like the kakapo parrot and the takahe, a threatened rail) to understand the host-microbe relationship and to use this information to help conserve these species.
Kevin R. Theis - Wayne State University - The Theis lab is very interested in how the microbiome can shape animal behavior, and vice versa.
Irene Tieleman - University of Groningen - The Tieleman lab investigates what role the environment plays in shaping the microbiome of birds, and how in turn the microbiome shapes their physiology and ecology. Dr. Tieleman also asks if wild chicks inherit their microbiomes from their mothers through the eggs that they develop in.
Glossary
- Genome: DNA provides all of the information necessary for an organism to function. A genome is the complete set of genetic material (DNA) present in an organism.
- Host: a living plant or animal that provides a guest organism with a place to live either on or within their body
- Microbiome: refers to the microbiota's collection of genomes (DNA) or transcriptomes (RNA) within a host
- Microbiota: a collection of microorganisms living within a host
- Physiology: the study of how an organism's body functions
- Sequencing techniques: a series of steps to extract and isolate genetic material, identify the specific DNA and RNA combinations of the target organisms
- Stopover: places where birds stop flying to rest and refuel during migratory journeys
- Transcriptome: RNA transcripts are a copy of select DNA sequences that an organism uses to construct functional products (e.g. proteins) needed at that specific time. A transcriptome is the complete set of RNA transcripts produced by the genome at a given time.
Thank you to Steve Brenner for providing songbird photographs to illustrate this backgrounder.
Additional Resources
Credits:
Created with images by Clara Cooper-Mullin • SK Yeong - "Eurasia Tree Sparrow" • ractapopulous - "bird owl eyes" • homecare119 - "bird wings fluttering"