Comparison of Human gut Microbiota with other Animals

 

Sanjana Subramanian, Haripriya Thiruvengadamani, Mythili Sathiavelu

School of Biosciences and Technology, Vellore Institute of Technology, Tamil Nadu, India.

 

ABSTRACT:

The gastrointestinal tract of humans has trillions of bacteria, which are of vital importance to the proper functioning of the body. They are not only essential for the digestion and absorption of nutrients, but even play a part in the immune system and metabolism of humans. For instance, it has been observed that the microbiome of healthy individuals is significantly different from those of diseased individuals. Across all species, the commonly occurring bacterial phyla in the GI tract are Bacteroidetes, Firmicutes and Proteobacteria. However, the proportion of these phyla have great diversity across species. In this review, we examine the similarities and differences between human gut microbiota with those of other animals and also the reasons for gut microbiota diversity, observing factors such as age, diet, and disease. By analyzing and observing such variations, effective treatments for GI diseases can be developed, common evolutionary history between species can be ascertained and developing healthy gut microbial environments may be possible.

 

 

INTRODUCTION:

The animal kingdom is extremely vast and diverse, yet many common features regarding microbiomes appear on comparison. Even very simple organisms such as nematodes have gut microbiomes. Therefore, restricting comparisons only to those species which are closely related to humans would be limited. Despite this fact, most studies on the gut microbiome have been conducted on mammals. In this review, the human gut microbiome has been compared with those of animals from the following phyla: nematoda, arthropoda, mollusca and vertebrata. Among vertebrates, further comparisons have been made between humans and other mammals, along with birds, fish, amphibians and reptiles. The animals which have been compared to humans are: C. elegans, bees, snails, cows, horses, dogs, cats, wood mice, macaques, chimpanzees, cottonmouth snakes, Burmese pythons, freshwater fish, Northern leopard frogs and chickens, along with other bird, insect and reptilian species.

 

Many factors such as the genetic components of the host immune system and external factors like the host’s diet and geography inform the similarities and differences between human and other microbiomes. The human gut microbiome has a great deal in common with other mammalian microbiomes, due to the similar structure of the organs of the digestive system, which will have similar pH and other properties, allowing the same species of bacteria to flourish. Additionally, as animals may be classified into herbivores, carnivores and omnivores, the composition of food which is digested varies. Hence, the bacteria which secrete enzymes and perform metabolic functions to digest and absorb the broken-down food particles will also vary, depending on the proportion of fats, proteins and carbohydrates taken in the diet.

 

Human microbiome:

The human gut microbiota has evolved in such a way that their densities vary across the gastrointestinal (GI) tract. The stomach has low density at 10^2-3 cells/ml while the colon has 10¹¹ cells/ml. The bacteria found in each part of the digestive system are also different. The mouth has Gemella, Streptococcus, and Lactobacillus. The stomach has a great amount of Helicobacter pylori (which is especially suited for survival in the low pH stomach), while the small intestine contains Escherichia, Enterococcus, Clostridium, Klebsiella, Bacteroidetes, and Ruminococcus. The large intestine has five major phyla of bacteria: Firmicutes, Actinobacteria, Proteobacteria, Verrumicrobia and Bacteroidetes. These vary in proportion across the human population. The large bacterial population of the large intestine is due to lower acidity and bile salts, the high volume of the large intestine and the longer retention time of the digested food. The bacteria can be classified as autochthonous (those with niches) and allochthonous (those without niches). These bacteria are involved in functions such as saccharolysis, sugar and amino acid fermentation and utilization and methanogenicity¹. The growth of these bacteria may have been through natural selection. It is thought that the development of agriculture and the addition of starch and milk to diets changed the microbiome².

 

The microbiome of humans is inherited from the mother at birth. This even varies among babies delivered naturally and via C-section, with C-section newborns having gut bacteria associated with skin and mouth while naturally delivered ones do not³. Identical twins have more similar microbiomes than fraternal twins⁴. The human gut microbiome has three different enterotypes (high amount of Prevotella and Bacteroides and Firmicutes in the background, high amount of Firmicutes and lesser amounts of Prevotella and Bacteroides, high amount of Bacteroides and low amounts of Prevotella and Firmicutes)². The composition of gut microbiota fluctuates during infancy. Within the first few days after birth, Firmicutes is the most predominant. Within 98 days after birth, Actinobacteria is the most common. During 371-413 days after birth, Firmicutes and Bacteroidetes take up a similar share of the microbiome, followed by Bacteroidetes taking first place and Firmicutes in second place. All other species have small percentages by this time⁵. Breast milk may also play an important role in microbiota assembly⁶. Additionally, malnutrition in the mother may delay the microbial metabolism of the infant or make it immunodeficient and unable to handle pathogenic bacteria².

 

The gut microbiome attains an adult-like composition in children even by the age of 3 and the greatest variation of gut microbial communities is during childhood. Microbiota varies between people of different countries across different ages, such as between Americans, Malawians and Amerindians. Diversity in the microbiome also generally increases and changes with age. For example, some bacteria (such as Bifidobacterium, Lactobacillus, Lactococcus and Streptococcus) are common in babies but not in older individuals. Western diets shape the bacterial colonies in the gut. Genes such as for alpha-fucosidase are predominant in the USA individuals because their diets are rich in sugars, while urease is higher in the Malawian and Amerindian populations, who have maize and cassava diets. Hence, bacteria which possess the urease gene are more common in these populations (e.g. S. thermophilus and S. infantarius). Additional differences arise due to the high amount of protein in American diets. Enzymes needed to break down amino acids are found in the American microbiomes compared to Malawians and Amerindians, who have a greater proportion of enzymes which break down carbohydrates⁷. High fat, protein and meat diets bring about Bacteroidetes dominance while high carbohydrate and meatless diets will bring about Prevotella dominance^1,3,6,8,9,10. Additionally, even one day of changing the diet rapidly alters the microbiota⁸.

 

A healthy human microbiome forms the core microbiome of humans. 18 species of bacteria are common in individuals from Spain and Denmark, and furthermore, over 90% of the 124 subjects studied have the same 57 species and 50% of the subjects have the same 75 species¹¹. Bacteroidetes thetaiotamicron is in 47% of subjects. Despite this, there is a great deal of variation among individuals, and core microbiomes may vary across continents, age, sex, and diet. The microbiome should remain stable to maintain the health of the human body. Artificially altering the microbiome using antibiotics is highly undesirable and may be associated with diarrhoea, colitis, abnormal metabolism and gastrointestinal disorders. Probiotics and prebiotics can combat dysbiosis and cause the growth of a microbial community with a positive impact on the digestive system².

 

The human microbiome composition is mostly of Firmicutes (53.9%), Bacteroidetes (35.3%) and Proteobacteria (4.5%). Other bacteria are present at less than 2% (Verrumicrobia, Actinobacteria, Tenericutes)⁴, and this composition varies with disease.

 

In colorectal cancer patients, the Bacteroidetes phylum percentage is 6.3% higher while Firmicutes phylum percentage is 6.3% lower¹². Among Firmicutes, the Gram-positive class Clostridia, which is responsible for fiber fermentation and a possible inflammation inhibitor and carcinogen inhibitor, suffers the greatest depletion. Gram-negative Fusobacterium and Porphyromonas percentages are also greater among colorectal cancer patients than control patients¹². Patients with multiple sclerosis have dominant levels of Firmicutesand Bacteroidetes which corresponds with an altered immune transcriptome¹³.

 

Vertebrate Microbiomes:

Other mammalian microbiomes:

Mammalian microbiomes form clusters based on diet; 65.7% of the sampled mammal microbiomes were of Firmicutes, and 16.3% being Bacteroidetes², showing the close relationship between the microbiota of all mammals. Gut bacteria are very different from free-living bacterial communities. Herbivores have the greatest microbial diversity and carnivores the least amount of bacterial phyla. Herbivores can be split into two groups, foregut fermenting (group 1) and hindgut fermenting (group 2). Omnivores can be split into hindgut fermenting and simple gut groups. Mammals form clusters based on their diet. Sometimes mammals do not match within their own group, but show more similarities to others (such as red pandas having carnivore-like microbiomes despite being herbivores)^2,14. Mammals living in captivity deviate from these findings¹⁵. Herbivores tend to have greater microbial diversity than predatory carnivores⁵. Obligate scavengers have the greatest amount of stomach acidity, which evolved as a filter to prevent pathogenic access to the gut and also to lyse the proteins present in meat with enzymes such as protease. Herbivores tend to have less acidic stomachs due to the need for fermentation-enabling bacteria which digest cellulose and lignin¹².

 

Related primate species include the macaque, chimpanzee and bonobo. The rhesus macaque's intestinal microbiome, similar to humans, the rhesus macaque microbiome is mostly Firmicutes, Bacteroidetes and Proteobacteria. However, other microbiota vary greatly. Helicobacter and Spirochaetes (especially Treponema) are of a greater proportion in macaques while Verrumicrobia and Actinobacteria do not¹⁶. There are many anaerobic bacteria in the macaque GI tract as well, such as Proteobacteria¹⁷. In macaques, the strains of these bacteria differ between males and females. Colitis-suffering macaques are more likely to have Campylobacter¹⁷.

 

The chimpanzee microbiomes have sorted themselves into enterotypes, just as human microbiomes do. Chimpanzee enterotypes can be categorized into: Bacteroidetes, Faecalibacterium and Parabacteroidetes (group 1), Lachnospiraceae (group 2), Dialester, Ruminococcus, Subdoligranulum and Colinsella (group 3). Despite these similarities, chimpanzees have a greater abundance of bacteria which are present only in low quantities in humans. These include bacteria such as Bifidobacteria, Acetovibrio, and Bulleidia. Unlike in humans, who have Prevotella-dominant microbiomes when they eat a carbohydrate-rich diet, chimpanzees always have Prevotella-dominant microbiomes because they always have a carbohydrate-rich diet¹⁰.

 

Other mammals such as cats and dogs have the same dominant bacterial species as humans, such as Firmicutes, Proteobacteria, Bacteroidetes, and Actinobacteria. Enterobacteriaceae are common in both cats and dogs. Similar to humans, when they are treated with antibiotics, their microbiome composition also changes. Besides bacteria, archaea, yeasts, molds and viruses live in the GI tract of cats and dogs. Their gut microbiota also acts as a shield against pathogens and provides digestive enzymes for nutrient utilization^18,19.

 

There is less knowledge about the cat gut microbiome compared to other companion animals. However, some studies into the cat gut microbiome have still been conducted. Within cats, Firmicutes is the most prevalent. Unlike in humans, Proteobacteria is the second most common while Bacteroidetes is only the third most prevalent¹⁹. 84% of cats have Bifidobacterium. Cats also have a greater concentration of bacteria in certain parts of GI (such as duodenum) compared to humans¹⁸.

 

In dogs, Firmicutes and Bacteroidetes are the majority of the microbiome. In gene sequencing, 63% of dog reads match the human gene catalog. The dog gut gene pool matches the human microbiome by 26%, showing the great similarities of these two microbiomes. Dogs, when fed a high protein low carbohydrate (HPLC) diet, have a greater shift in their microbiomes than the reverse diets of low protein high carbohydrate (LPHC). Similar to humans, the dogs fed on LPHC have a higher Prevotella to Bacteroidetes ratio than the HPLC dogs. Overweight dogs have a more sensitive microbiome, while L. ruminis is not present in HPLC fed dogs²⁰.

 

Wood mice have a dominance of Firmicutes (52.1%) and Bacteroidetes (37%) with Proteobacteria (8.2%) being the third most common bacterial phylum. Other phyla such as Tenericutes and Actinobacteria are present only in small percentages. Among wood mice, the composition of the microbiome varies between the seasons. This is due to the shift in diet from a plant diet in the spring and early summer to an insect diet in the late summer and fall. Lactobacillus is found in the gut microbiome at springtime while Helicobacter and Alistipes are common during fall²¹.

 

Mammals which have rumens such as cows may also have core microbiomes. Cows have an abundance of Bacteroidetes (32.8%), Firmicutes (43.2%) and Proteobacteria (14.3%). Cows consuming a forage diet rich in fiber have high quantities of Fibrobacter, Ruminococcae, Saccharofermentans and Spirochaetes. In cows fed on grain and not forage, Prevotella was at high quantities instead, similar to humans and chimpanzees. This shows how diet plays a large role in microbial composition. Prevotella percentage seems to always correspond to high grain/carbohydrate diets. As with humans, the percentages of these bacteria all rise and fall along with a change in diet. Mixed forage diet cows had a greater proportion of Clostridiaceae and Prevotella. Similar to humans, bacterial composition changes with pH. Lactobacillus and Streptococcus were in abundance in acidic environments. One special quality of cows is that their rumens can return to stable conditions after an abrupt disturbance, such as sudden acidity. Their ability to maintain a stable gut microbiome may be important in preventing infections²². The cow microbiome fluctuates with age²³.

 

The horse has also been the subject of gut microbiome analysis. Firmicutes are the most common in the intestine, as well as being the most common in the stomach. The stomach also has the acidic conditions needed for Lactobacillus. Verrumicrobia are in the small colon, rectum and feces and Proteobacteria are found in the duodenum. Together, they are very common in the large intestine. Spirochaetes are also in feces. Like cows, horses also have Fibrobacter (present in large and small colon and feces). Bacteroidetes are in the cecum, small colon and feces. Horses also suffer from changes in the GI microbiota when they have diseases such as colitis, or during antibiotic treatment²⁴. Microbiota vary between different parts of the gastrointestinal tract, such as between the caecum, colon and feces²⁵.

 

Table 1: Mammalian Gut Microbiota Comparison

 

Fish microbiomes:

Fish gut microbiomes contain Proteobacteria (mainly Gammaproteobacteria) and Tenericutes (a branch of Firmicutes). The aquatic environment^26,27 and fish size play a major role in the acquisition of the microbiota. However, commercially important fish have huge amounts of Fusobacteria and their first feeding affects their gut bacterial composition. Actinobacteria, Firmicutes and Bacteroidetes also appear in fish microbiomes²⁸.

 

The high prevalence of Tenericutes and Proteobacteria distinguish fish microbiomes from mammals^26,27.

 

Trophic level and time of sampling changes their gut microbiome. For example, grass carp from artificial ponds in the Yangtze River had Proteobacteria, Actinobacteria, Cyanobacteria and Firmicutes. Grass carp from Dongxihu Fish Farm had Firmicutes, Fusobacteria, Proteobacteria and Bacteroidetes. Herbivorous fish have higher levels of Proteobacteria than carnivorous, omnivorous and filter-feeding fish and that Firmicutes is the second most common phylum. Carnivore fish have a greater amount of Fusobacteria and herbivorous and omnivorous fish have a higher amount of Clostridium, a cellulose-degrading bacterium. However, there was no significant difference in cellulose-degrading bacteria between omnivores and filter-feeding fish. Herbivores also had a higher amount of amylase activity than carnivores, and carnivores had a greater amount of trypsin activity than herbivores. In fish as well as other vertebrates, carnivores have the least diversity, as they have the least unique operational taxonomic units (OTUs)²⁹. Under starvation, Asian seabass’ intestinal Bacteroidetes population increases by 27.8%. Additionally, the Gamma proteobacteria level is increased in the intestinal microbiome of Asian seabass³⁰.

 

Amphibian microbiomes:

Amphibians undergo a life cycle which includes metamorphosis, which alters their microbiome^28,31. There are many tadpole-specific bacteria, such as Acidobacteria and Shewanella. These all disappear by the time they reach maturity. Some bacteria are completely absent in tadpoles, but appear in frog microbiomes, such as Akkermansia. Tadpoles have greater phylogenetic diversity than frogs, possibly due to diet. Tadpoles are herbivores while frogs are insectivores with high-chitin diets. Other factors are oxygen tolerance of bacteria such as Proteobacteria, formation of stomachs and changing pH and epithelial cells in the GI tract³².

 

Tadpoles, including Northern leopard tadpoles have a Firmicutes and Proteobacteria microbiome, while adult frogs have mostly Bacteroidetes and Firmicutes. Their Verrumicrobes and Proteobacteria populations significantly decrease, and Actinobacteria and Acidobacteria also seem to decrease³³.

 

The bacterial phyla of the tadpole gut changes with temperature. The Proteobacteria population increases greatly with cool temperatures and decreases with warm temperatures, while Firmicutes population moderately decreases in warm temperatures. The Actinobacteria population is higher in warm temperatures, and the Planctomycetes population does not exist in cool conditions, but greatly increases with temperature. Mycobaterium also increases in warm conditions. Tadpoles raised in cool temperature are less taxonomically rich compared to those raised in warm temperatures³³.

 

Reptilian microbiomes:

Gopher tortoises have an equal amount of Bacteroidetes and Firmicutes. American alligators have different concentrations of microbiota in the upper GI tract (Proteobacteria) and lower GI tract (Firmicutes and Fusobacteria)²⁸.

 

Crotaline snakes surveyed previously had Bacteroidetes and Firmicutes-prominent microbiomes, varying by the part of the GI tract studied. The cloaca and small intestinal microbiomes of the crotaline snakes had mostly Proteobacteria (specifically Gammaproteobacteria). In the cloaca, the Firmicutes and Bacteroidetes are second and third place, while this is reversed in the case of the small intestine. However, in the large intestine, Bacteroidetes is the majority, followed by similar numbers of Firmicutes and Proteobacteria²⁸.

 

The Burmese python also has Bacteroidetes and Firmicutes-dominated microbiomes. But a different pattern is observed within them; during feasting and fasting, the numbers of these two phyla change. Firmicutes are prominent during feasting while Bacteroidetes numbers increase during fasting. The fasting period also has high amounts of Proteobacteria, Deferribacter and Verrumicrobia. Within the Burmese python’s GI tract, bacterial compositions of the small and large intestines are similar. But in the cottonmouth (crotaline) snake, Proteobacteria outnumbers others in the SI and cloaca while Bacteroidetes outnumbers the other phyla in the LI³⁴. Burmese pythons undergo such changes because they have a feeding habit of fasting for long periods of time (one month or more), followed by digestion of prey which is often 25-50% of the snake’s body mass. When feeding time arrives, the snake’s internal organs enlarge drastically and digestive enzymes are secreted. Digestion often takes 1-2 weeks to complete. Due to this, gut microbiota have to adjust themselves accordingly^28,35.

 

Avian microbiomes:

Bird microbiomes differ depending on their captivity. Actinobacteria, Clostridiales and Synergistetes are much more common in wild than in captive birds, who have more Gammaproteobacteria. Avians have Firmicutes-dominant microbiomes^36,37.

 

Diet and digestive system alters the gut microbiome. The hoatzin, which feeds on leaves, has a microbiome similar to a cow’s, due to having an enlarged crop. Its microbiome is mostly Bacteroidetes, Firmicutes and Proteobacteria. Scavenging birds like vultures are immune to toxin-producing bacteria and have diverse microbiomes of Actinobacteria, Proteobacteria and Firmicutes. The vulture hindgut has large numbers of Clostridium and Fusobacteria, which have contain some toxic species that the vulture can tolerate. Fusobacteria is often found in carnivorous and omnivorous birds³⁷. Carrion feeding birds have increased stomach acidity compared to birds which eat insects, fruit, and leaves³⁸.

 

In the ostrich gut microbiome as well, Clostridia and Proteobacteria were found to be dominant in the caecum, colon and feces. However, the cloaca and ileum differed. The cloaca had mostly Gammaproteobacteria, Bacilli and Clostridia. The ileum had mostly Betaproteobacteria and Bacteroidetes³⁹.

 

Birds which are used as model organisms or which are part of the poultry industry, such as chickens, are often more widely studied than other avians^40,41,42. Avians tend to have Firmicutes-dominant microbiomes³⁷. Specifically, chicks’ GI tract is most abundant in Firmicutes, followed by Bacteroidetes and Proteobacteria^42,43. This changes in adults as Bacteroidetes dominates⁴². Yet, the concentration of each of these varies by location in the intestines. The gizzard of the chicken mostly has Lactobacillus, Enterococcus and Clostridia⁴³. The chicken caecum has, like most vertebrates, mainly Firmicutes, Bacteroidetes and Proteobacteria^.43. The chicken microbiome has pathogens capable of infecting humans, such as Salmonella and Campylobacter. These either have no harmful effect on the chicken or are opportunistic pathogens⁴².

 

Invertebrate Microbiomes:

Insect microbiomes:

Not many studies have been performed to understand the gut microbiomes of insects as a group. Instead, individual species of insects have been studied. Insect gut microbiomes are mainly dominated by Proteobacteria (62.1%), Firmicutes (20.7%) and Bacteroidetes (6.4%). Others are Actinobacteria and Tenericutes as well as some unclassified bacteria. There are some exceptions to this, with some species having Bacteroidetes, Tenericutes, and Actinobacteria, as the dominant ones. The Wolbachia genus is highly prevalent as well. 60.7% of the genera were aerobes while the remaining were anaerobes or facultative anaerobes. These proportions varied based on the habitat and diet of the insects. Terrestrial insects had more aerobic bacteria than aquatic ones. Omnivores had greater diversity of bacteria compared to herbivores and carnivores⁴⁴. pH also alters the microbiota composition⁴⁵.

 

Some insects, such as caterpillars, do not have a gut microbiome or have microbiota only in very low quantitiesbecause their GI tract does not allow their growth. Instead of relying on resident microbiomes for digestion, they secrete their own digestive enzymes, high pH and disruption to complete digestion. Individuals with simple GI tracts have less diverse microbiomes as well⁴⁶.

 

Honey bees have five main bacteria forming most of their community. These are Snodgrassella alvi, Gilliamella apicola from Proteobacteria, Lactobacillus from Firmicutes and Bifidobacterium asteroides from Actinobacteria. They have the same dominant phyla as humans, but they are much simpler and have a few specific bacteria as their core gut microbiome. Differences occur between queens, drones and workers and between ages. These bacteria have a similar role to those in humans and other mammals and assist in carbohydrate fermentation and sugar utilization. This is due to the bees’ high-carbohydrate diet⁴⁷.

 

Snail microbiome:

The giant African snail has dominant Proteobacteria in the crop fluid and Firmicutes and Bacteroidetes in fecal samples. They have large amounts of Sulforospirillum, which is from Epsilonproteo bacteria. In snails fed sugarcane, Bacteroidetes decreases by 50% while Firmicutes increases. This is seen in obese humans, mice and pigs as well⁴⁸.

 

Caenorhabditis elegans microbiome:

C. elegans, a nematode, has mainly a Proteobacteria-rich gut microbiome, further classified into Enterobacteriaceae of the Pseudomonas and Sphingomonas. Their gut microbiomes also contain Firmicutes, Bacteroidetes and Actinobacteria. External bacteria are able to enter the nematode gut. Some, such as Ochrobactrum, are very persistent in surviving in the nematode gut despite adverse conditions. Microbiota such as Pseudomonas even demonstrate anti-fungal activity. This may be proof that they function as immune responses in nematodes^{49, 50}.

 

Table 2: Gut Microbiota Across Class/Phyla.

 

DISCUSSION:

The gut microbiomes of various animal phyla are all demonstrated to be mainly composed of three major bacterial phyla: Bacteroidetes, Firmicutes and Proteobacteria. However, the specific species of bacteria vary across the animal kingdom, across individuals of the same species and even the same individual through the passage of time. The causes of these changes are often, but not limited to: seasonal variation, disease, change in diet, temperature, antibiotics and so on. By comparing the variations among different microbiomes, it could be possible to understand the causes of diseases create medicines and treatments against diabetes, cancers and gastrointestinal disorders such as colitis and learn how to develop a favourable environment for the growth of beneficial bacteria so that human health and longevity can be improved.

 

ACKNOWLEDGEMENT:

The authors thank the management of Vellore Institute of Technology, Vellore for providing the necessary support in completion of this review.

 

CONFLICT OF INTEREST:

The authors declare no conflict of interest.

 

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Accepted on 25.04.2022           © RJPT All right reserved

Research J. Pharm. and Tech 2022; 15(12):5541-5547.