Whales prove to be a very interesting and unique clade of mammals from many angles, be it their evolution towards fully-aquatic lives, feeding strategies, gigantism, sensory adaptations, or cognitive abilities. Now as the study of microbiomes adds new dimensions to understanding animals, whales continue to stick out.
Quick intro to microbiomes
I should provide a crash-course for those not too keen on microbiology before heading into the crux of this post. A microbiome is the collection of microorganisms or the total amount of microbial genetic material in an environment. Not only are microbiomes defined in environments like soil and bodies of water but also within multicellular hosts like plants and animals. Microbiomes are often defined on the skin, respiratory tracts, blood, and digestive tracts of humans and animals. Microbiomes can be vital because they often regulate the health of the host species they inhabit. These roles can vary from aiding digestion or out-competing invading pathogens for resources. Research into characterizing microbiomes in humans and other species is a relatively recent practice compared to other fields such as anatomy, behavior, and genetics. We’re now learning that this overlooked character is extremely important.
When assessing microbiomes, we use similar metrics discussed in ecology: richness, eveness, and function . Richness is simply the number of species present in an environment. Eveness is the relative abundance of each species, and this value can be combined with richness to calculate the diversity within a microbiome. Function includes a microbe’s niche, typically the type of molecules they break down. Diversity and function are measured by collecting samples from the microbiome (methodology varies with the environment being sampled), extracting the DNA/RNA from the microbiomes, amplifying desired sequences, sequencing the genetic material and aligning the informative regions to reveal the identity of species present. There’s a lot more to the process such as filtering out contamination, separating high and low-quality sequences, etc. With the resulting data, the taxonomic composition of a microbiome becomes available. Functional profiles are provided by measuring the expression of specific genes within the samples. The results of these procedures can vary depending on the precise methodology and equipment used.
When characterizing a host species’ microbiome, we look for core assemblages, which are the bacterial taxa that are mutually shared between the majority or the entirety of the population. Core assemblages are important to define for host species, as deviations from the core assemblage of a species or population can infer a major health risk. Therefore, microbiome samples should be a priority for conservation research.
This post will focus on the gut microbiomes, which are most often analyzed from fecal samples. A key concept about the gut microbiome is that it’s often controlled by diet, as the type food the host consumes provides the nutrients available to the bacteria. Another component is the evolutionary history of the host. Host phylogeny matters because the anatomy and physiology of the GI-tract is the literal environment in which the bacteria must thrive. The consequence of this is what’s known as phyolgenetic intertia, the retention of the ancestral gut microbiome even after adapting to a unique diet. A classic example is the giant panda, which lacks a microbiome that’s enriched with the bacteria typical of other herbivores. Instead, the giant panda’s microbiome clusters with other ursids and carnivores (1). This is because the panda’s GI-tract is simple and lacks the multi-chambered adaptations present in ruminants, horses, and rabbits. Pandas are still ”carnivores” with respect to their digestive anatomy. Since both anatomy and diet shape the host’s hospitability for microbes, gut microbiomes can change within the same host over the course of time or across different sections of the GI-tract.
The gut microbiomes of cetaceans
Now to finally bring this conversation back to whales. Those who are familiar with their evolutionary history, as discussed in my Cetology 101 article, can see where I am going. Whales are strict carnivores, but since they are deeply-nested within artiodactyls, their terrestrial ancestors were herbivores at some point. Therefore, whales occupy an extremely interesting dietary niche with respect to their phylogeny. This is especially true in the case of baleen whales. Baleen whales consume crustaceans like euphausiids (krill), copepods, amphipods, mysids, etc. The exoskeletons of these animals are composed of chitin, which is a structural polysaccharide (long-chained sugar) like the cellulose consumed by herbivores. Chitin and cellulose are both composed of chains of glucose, like starch. However, the bonds linking the glucose molecules in chitin and cellulose are much stronger, making these molecules harder to digest than starch.
Ruminants break down cellulose with the aid of the microbiome within their forestomach. The upper digestive tract of ruminants has 4 chambers: the rumen, reticulum, and omasum, and abomasum. Of these, only the abomasum is the true homolog to the stomach, the rest are derived from the esophagus. The rumen and reticulum house microbes that are capable of breaking down cellulose and the omasum passes food particles to be digested in the abomasum. This process is known as foregut fermentation. Cetaceans also possess a forestomach, however this structure is not believed to be homologous to the pregastric chambers of ruminants as the cetacean forestomach is derived from the true stomach. Nonetheless, this structure was likely an analogous fermentation chamber of cellulose in the ancestors of whales that may have been converted to do the same for chitin. Preliminary evidence for this hypothesis was the detection of high concentrations of short-chained fatty acids (SCFA’s) in the forestomaches of baleen whales (2). SCFA’s, for the purpose of this discussion, are products from the fermentation of carbon sources.
(Click on caption of diagram below for full description)
As mammalian carnivores that possess anatomically-herbivorous digestive tracts, the gut microbiome of cetaceans present a unique opportunity to understand how diet and phylogeny interact. This is not mirrored by any other marine mammal, as Sirenians and Pinnipeds both occupy dietary niches that align with their ancestral digestive anatomy. Work has been done into cetacean microbiomes over the past half decade, but the science remains immature. Nonetheless, I will provide the basic summary of what we currently know.
In 2015, researchers conducted a taxonomic and functional comparison between the fecal microbiomes baleen whales and terrestrial mammals. They concluded that the microbiomes of baleen whales were very unique, possessing qualities of both carnivores and herbivores. At the phylum-level, the fecal microbiomes of baleen whales were very similar to those of terrestrial mammals, dominated by Bacteroidetes and Firmicutes (2). Bacteroidetes and Firmicutes make up the majority of the gut microbiome in most mammals, including humans. However, whales still had some enrichments in bacterial phyla that were uncommon in terrestrial mammals (Spirochaetes). At the species-level, the similarities with terrestrial mammals decreased greatly.
Functionally, the fecal microbiomes of baleen whales were similar to carnivores for genes related to digesting and synthesizing proteins. However, baleen whales and herbivores were much closer for genes involved in carbon and lipid metabolism. Baleen whales grouped independently from both terrestrial carnivores and herbivores for carbohydrate metabolism. This meant that whales and herbivores broke down sugars differently (which is to be expected because chitin and cellulose are different sugars), but all the downstream steps for breaking down the lower-level carbon molecules were the same. This is consistent with the hypothesis of chitin-fermentation.
Another notable finding were the carbohydrate-active enzymes (CAZymes) profiles for the microbiomes of baleen whales. CAZymes are genes involved in the digestion of carbohydrates. The CAZy profiles of the baleen whale microbiomes were unique from those of terrestrial mammals (2). Baleen whales even lacked affinity with insectivores, whose prey also possess chitinous exoskeletons. Despite feeding on insects, insectivore gut microbiomes were not enriched in genes related to chitin-digestion when compared to the average carnivore. Baleen whales, however, were particularly enriched in these very genes. Like in the situation of the panda, this pattern is likely due to the insectivores having simple digestive anatomy, while whales inherited a forestomach capable of housing chitin-fermenting bacteria.
The microbiome analyses firmly support that baleen whales engage in the foregut fermentation of chitin, paralleling their ruminant relatives. Dolphins and porpoises on the other hand, clustered with other marine piscivores. Studies of the fecal microbiomes of the bottlenose dolphin, striped dolphin, and East Asian finless porpoise were all found to be largely enriched by the bacterial phyla Firmicutes and Proteobacteria (3,4,5,6). The lineages within Proteobacteria were related to those found in piscivorous marine fish, indicating a convergence from their shared dietary niche (7). Belugas were somewhat different, as their microbiomes were enriched in Actinobacteria. This is odd, as belugas belong to a sister clade to porpoises and share a similar diet. Differences in their environments might be the key here. Porpoises and dolphins generally live in lower latitudes, while belugas live in Arctic and subarctic waters. This explanation is supported by the gut microbiome of the hooded seal, which had a far greater relative abundance of Actinobacteria relative to Proteobacteria (8). As of yet, precise functional profiles for toothed whales are not as extensive as they are for baleen whales.
It seems that, in general, toothed whales overcame their phylogenetic inertia and aligned with piscivores, right? Well, this is where sperm whales come in to make this whole thing weird. The taxonomic profiles of the true, pygmy, and dwarf sperm whales revealed their microbiomes cluster much more closely to baleen whales than to other toothed whales. Like baleen whales, Bacteroidetes and Firmicutes were the dominant phyla in all three sperm whale species, but the Kogiids’ microbiomes were distinct from baleen whales for lower-abundance phyla (9,10,11,12). No significant differences were found between the fecal microbiomes of baleen whales and the sperm whale (Physeter macrocephalus) at the phylum-level, only at the family/genus-level (12). Furthermore, some of the lineages detected in Kogiids were associated with fermentation, which is consistent with previous analyses of the bile acid in sperm whales (9).
I think these preliminary similarities between baleen whales and sperm whales are striking when taking into consideration of their phylogeny. Baleen whales and toothed whales diverged about 36-37 million years ago, while sperm whales diverged from other odontocetes 32-35 million years ago (13, figure below). So while sperm whales are more closely related to dolphins and belugas than they are to baleen whales, the sperm whales’ ancestors were a very basal odontocete lineage. While the precise phylogeny of fossil physeteroids has yet to be fully resolved, it may be possible that the ancestor of the teuthivorous sperm whales had similarities to the ancestors of mysticetes. This may be possible, as early mysticetes are believed to have been suction-feeders, much like sperm whales (14).
(Click on caption of diagram below for full description)
But their phylogeny still fails to answer precisely why the fecal microbiomes between modern sperm whales and baleen whales are so similar. Is it some anatomical similarity between these clades, or is there something we’ve overlooked regarding their diets? I believe it’s definitely worth noticing that the pens and beaks of squids are composed of chitin. This idea may seem counterintuitive for some sperm whale experts, as the beaks and pens of squid are often recovered undigested. However, it’s too distracting that the gut microbiomes of sperm whales, who feed on chitin-rich prey, cluster more closely to a group whose microbiomes are geared towards chitin. A supporting detail is that one isolate from the Kogiid fecal microbiome showed visible utilization of chitin (10). This may hint at some weak chitin digestion in sperm whales. If not necessarily for nutritional purposes, it may serve as a defense mechanism to protect the GI-tract, like ambergris. More research in the functional profiles of sperm whale microbiomes is necessarily to make sense of all of this.
So in general, we see the following trend across cetaceans. Baleen whales and sperm whales have microbiomes that share taxonomic affinities with terrestrial herbivores and are functionally skewed towards fermentation. Other odontocetes such as dolphins, porpoises, and belugas have microbiomes convergent with typical marine piscivores. Until more information is acquired, the shared exposure to chitin-rich prey seems to explain the fecal microbiome homology between baleen whales and sperm whales .
(Click on caption of diagram below for full description)
Limitations of current research
Even though we’ve learned a lot so far in the past half-decade, there’s still so many gaps to fill regarding cetacean gut microbiomes. I’d say the biggest shortcoming of the existing research is the taxon sampling. Every cetacean species with published gut microbiome data is present within my bibliography (this article is based on a literature review I’ve done for my microbiology class). Among these, not a single beaked whale has been sampled, which is problematic.
The beaked whales’ inclusion is very necessary in the discussion of phylogenetic inertia’s role in cetacean gut microbiomes due to unique features of their anatomy. In accordance to their general weirdness, beaked whales lack forestomaches (15)! It should be of great interest to obtain a fecal sample of the beaked whales and observe how their gut microbiomes align or deviate from other cetaceans. Specifically, they ought to be compared with sperm whales, as they share the closest dietary niches. Accordingly, we should also prioritize sampling the polyphyletic clades of river dolphins, as the Yangtze river dolphin and the La Plata dolphin also lack forestomaches (16). While the former is extinct, sampling of the La Plata dolphin may still yield information to make reasonable speculations.
Aside from the absence of beaked whales from the datasets, more analyses are needed from the currently-sampled species. The existing datasets for the gut microbiomes of toothed whales only includes taxonomic compositions . Preliminary functional profiles have only been obtained for baleen whale microbiomes. Furthermore, most species have only been surveyed through fecal samples. These can only provide a snapshot of the composition of the gut microbiome, and cannot properly elucidate how it’s structured throughout the different sections of the GI-tract. The gut microbiome of the esophagus and stomach can look very different from the colon. Indeed significant changes in taxonomic composition has been observed throughout the GI-tracts and life histories of the bottlenose dolphins, finless porpoises, kogiids, and bowhead whales (4,6, 10, 17).
Attention should also be paid towards the health and residency status of the specimen being sampled. Diseases or antibiotic treatments are liable to disturb the taxonomic composition of gut microbiomes collected from stranded specimens (18). As for residency status, researchers should avoid over-reliance on data collected from captive individuals, as major differences in core assemblages were found in wild vs captive comparisons (19).
All of these measures ought to be considered for any future research, as adherence will allow for stronger data that will make way for clearer patterns.
The bigger picture
I have established the gut microbiome’s importance within their hosts, but not at any greater scale. To gain perspective of how gut microbiomes ultimately affect the world at large, we must tie them back to how whales regulate the environment.
The ocean stores about 50 times as much CO2 as the atmosphere and absorbs around one-third of the carbon emitted by humans (20). There are multiple means the ocean removes CO2 from the air, but one of the major means is the biological pump. Basically, the biological pump describes how the primary producers like cyanobacteria and algae fix CO2 from the atmosphere and convert the carbon into organic matter. This organic matter is then stored into the bodies of the marine animals at higher trophic levels. When these animals die, their bodies sink to the bottom of the oceans and the carbon is stored into the ocean interior. Large vertebrates with few predators such as baleen and sperm whales play a very important role in the biological pump of the ocean. Larger animals require less food per unit of mass as smaller animals, meaning they are more efficient for storing carbon in the water (21). This means that if the Antarctic blue whales went extinct, the increase in biomass of Adélie penguins and minke whales in response to the new krill availability would only be a fraction of the lost blue whale biomass. We cannot count on an increase of smaller species to replace the carbon storage a larger animal once provided.
With this background of the biological pump in mind, the decimation of large cetacean populations from whaling should become very troubling. A study has calculated that the current populations of 8 species of large baleen whales (Blue, fin, humpback, gray, sei/Bryde’s, right, bowhead, and minke) are storing about 9.1 million less metric tons of carbon than during the pre-whaling era (21). If these populations were to be rebuilt to to their historical abundances, the oceans could store 8.7 million more metric tons of carbon. Furthermore, the carcasses from ”whale falls” is expected to allow the ocean to remove 160,000 more metric tons of carbon per year. While this may seem small compared to the total carbon sink of the ocean, restoring whale and fish populations is very comparable to other management projects, such as iron fertilization.
In addition to just storing carbon in their bodies, whales also support the oceans by guiding the cycling of nutrients. As whales return from deep-water foraging, they provide nitrogen and iron to phytoplankton when defecating at the surface (22,23). Furthermore, baleen whales transport nitrogen from nutrient-rich high-latitudes to nutrient-poor low-latitudes as they defecate along the migratory paths (24). Through these processes, whales act as both horizontal and vertical vectors of nutrients for primary producers of the ocean. Their carcasses also provide nutrients to scavengers at the surface and even full-on habitats for decomposers at the sea floor (25).
How does all of this relate back to gut microbiomes? Well, as mentioned before, these microbes are what allow a baleen whale to efficiently digest abundant carbon sources in the ocean such as chitin and a class of lipid known as wax esters. Like chitin, wax esters comprise a large proportion of the carbon in the ocean and is very difficult to digest for the majority of vertebrates. Whales and seabirds are the only vertebrates that showed high efficiency in digesting wax esters. The concentration of wax esters throughout the GI-tract of bowhead whales was shown to vary greatly with changes in the composition of the gut microbiome (17). Therefore, it’s very likely the gut microbiome plays a similar role in processing wax esters as they do with chitin.
All of the processes in which whales help manage the oceans are dependent on their ability to properly acquire energy and nutrients from their prey. Indeed, it is the smallest organisms that enable the largest animals to be major drivers of the biogeochemical cycling of carbon and nutrients of the ocean. Just as in other biological concepts, superlative nature of whales strongly illustrates the importance of microbiomes.
I hope this article proved interesting for readers despite possibly being my most technical paper as of yet. This article is basically a huge paraphrasing of two papers I’ve done for my senior year of undergrad. I really loved covering this topic for both semesters and I ended up learning so much. One of these papers was a literature review, and I pretty much copied that entire bibliography for this paper. So if you want to learn everything there is to know about the gut microbiome of cetaceans at this point in time, the sources below will essentially cover it with the addition of the following study (26).
- Xue, Z., Zhang, W., Wang, L., Hou, R., Zhang, M., Fei, L., Zhang, X., Huang, H., Bridgewater, L. C., Jiang, Y., Jiang, C., Zhao, L., Pang, X., & Zhang, Z. (2015). The bamboo-eating giant panda harbors a carnivore-like gut microbiota, with excessive seasonal variations. MBio, 6(3), e00022-00015. https://doi.org/10.1128/mBio.00022-15
- Sanders, J. G., Beichman, A. C., Roman, J., Scott, J. J., Emerson, D., McCarthy, J. J., & Girguis, P. R. (2015). Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nature Communications, 6(1), 8285. https://doi.org/10.1038/ncomms9285
- Morris, P. J., Johnson, W. R., Pisani, J., Bossart, G. D., Adams, J., Reif, J. S., & Fair, P. A. (2011). Isolation of culturable microorganisms from free-ranging bottlenose dolphins (Tursiops truncatus) from the southeastern United States. Veterinary Microbiology, 148(2), 440–447. https://doi.org/10.1016/j.vetmic.2010.08.025
- Godoy-Vitorino, F., Rodriguez-Hilario, A., Alves, A. L., Gonçalves, F., Cabrera-Colon, B., Mesquita, C. S., Soares-Castro, P., Ferreira, M., Marçalo, A., Vingada, J., Eira, C., & Santos, P. M. (2017). The microbiome of a striped dolphin (Stenella coeruleoalba) stranded in Portugal. Research in Microbiology, 168(1), 85–93. https://doi.org/10.1016/j.resmic.2016.08.004
- Abdelrhman, K. F. A., Ciofini, A., Bacci, G., Mancusi, C., Mengoni, A., & Ugolini, A. (2020). Exploring the resident gut microbiota of stranded odontocetes: High similarities between two dolphin species Tursiops truncatus and Stenella coeruleoalba. Journal of the Marine Biological Association of the United Kingdom, 100(7), 1181–1188. https://doi.org/10.1017/S0025315420000983
- Wan, X.-L., McLaughlin, R. W., Zheng, J.-S., Hao, Y.-J., Fan, F., Tian, R.-M., & Wang, D. (2018). Microbial communities in different regions of the gastrointestinal tract in East Asian finless porpoises (Neophocaena asiaeorientalis sunameri). Scientific Reports, 8(1), 14142. https://doi.org/10.1038/s41598-018-32512-0
- Huang, Q., Sham, R., Deng, Y., Mao, Y., Wang, C., Zhang, T., & Leung, K. (2020). Diversity of gut microbiomes in marine fishes is shaped by host‐related factors. Molecular Ecology, 29. https://doi.org/10.1111/mec.15699
- Acquarone, M., Salgado-Flores, A., & Sundset, M. A. (2020). The Bacterial Microbiome in the Small Intestine of Hooded Seals (Cystophora cristata). Microorganisms, 8(11). https://doi.org/10.3390/microorganisms8111664
- Erwin, P. M., Rhodes, R. G., Kiser, K. B., Keenan-Bateman, T. F., McLellan, W. A., & Pabst, D. A. (2017). High diversity and unique composition of gut microbiomes in pygmy (Kogia breviceps) and dwarf (K. sima) sperm whales. Scientific Reports, 7. https://doi.org/10.1038/s41598-017-07425-z
- Denison, E. R., Rhodes, R. G., McLellan, W. A., Pabst, D. A., & Erwin, P. M. (2020). Host phylogeny and life history stage shape the gut microbiome in dwarf ( Kogia sima ) and pygmy ( Kogia breviceps ) sperm whales. Scientific Reports, 10(1), 15162. https://doi.org/10.1038/s41598-020-72032-4
- Li, C., Tan, X., Bai, J., Xu, Q., Liu, S., Guo, W., Yu, C., Fan, G., Lu, Y., Zhang, H., Yang, H., Chen, J., & Liu, X. (2019). A survey of the sperm whale (Physeter catodon) commensal microbiome. PeerJ, 7. https://doi.org/10.7717/peerj.7257
- Glaeser, S. P., Silva, L. M. R., Prieto, R., Silva, M. A., Franco, A., Kämpfer, P., Hermosilla, C., Taubert, A., & Eisenberg, T. (2021). A Preliminary Comparison on Faecal Microbiomes of Free-Ranging Large Baleen (Balaenoptera musculus, B. physaus, B. borealis) and Toothed (Physeter macrocephalus) Whales. Microbial Ecology. https://doi.org/10.1007/s00248-021-01729-4
- Zurano, J. P., Magalhães, F. M., Asato, A. E., Silva, G., Bidau, C. J., Mesquita, D. O., & Costa, G. C. (2019). Cetartiodactyla: Updating a time-calibrated molecular phylogeny. Molecular Phylogenetics and Evolution, 133, 256–262. https://doi.org/10.1016/j.ympev.2018.12.015
- Lambert, O., Martínez-Cáceres, M., Bianucci, G., Celma, C. D., Salas-Gismondi, R., Steurbaut, E., Urbina, M., & Muizon, C. de. (2017). Earliest Mysticete from the Late Eocene of Peru Sheds New Light on the Origin of Baleen Whales. Current Biology, 27(10), 1535-1541.e2. https://doi.org/10.1016/j.cub.2017.04.026
Mead, J. G. (2007). Stomach anatomy and use in defining systemic relationships of the cetacean family ziphiidae (beaked whales). The Anatomical Record, 290(6), 581–595. https://doi.org/10.1002/ar.20536
Yamasaki, F., & Kamiya, T. (2017). THE STOMACH OF THE BOUTU , INIA GEOFFRENSIS: COMPARISON WITH THOSE OF OTHER PLATANISTIDS. https://www.semanticscholar.org/paper/THE-STOMACH-OF-THE-BOUTU-%2C-INIA-GEOFFRENSIS-%3A-WITH-Yamasaki-Kamiya/7d13b25aa7080324fcbb617a33600d61c5017081
Coordinated transformation of the gut microbiome and lipidome of bowhead whales provides novel insights into digestion | The ISME Journal. (n.d.). Retrieved October 26, 2020, from https://www.nature.com/articles/s41396-019-0549-y#Sec10
Bai, S., Zhang, P., Lin, M., Lin, W., Yang, Z., & Li, S. (2021). Microbial diversity and structure in the gastrointestinal tracts of two stranded short-finned pilot whales (Globicephala macrorhynchus) and a pygmy sperm whale (Kogia breviceps). Integrative Zoology, 16(3), 324–335. https://doi.org/10.1111/1749-4877.12502
Captive environment influences the composition and diversity of fecal microbiota in Indo‐Pacific bottlenose dolphins, Tursiops aduncus. (n.d.). https://doi.org/10.1111/mms.12736
Rackley, S. A. (2010). Chapter 12—Ocean Storage. In S. A. Rackley (Ed.), Carbon Capture and Storage (pp. 267–286). Butterworth-Heinemann. https://doi.org/10.1016/B978-1-85617-636-1.00012-2
Pershing, A. J., Christensen, L. B., Record, N. R., Sherwood, G. D., & Stetson, P. B. (2010). The Impact of Whaling on the Ocean Carbon Cycle: Why Bigger Was Better. PLoS ONE, 5(8), e12444. https://doi.org/10.1371/journal.pone.0012444
Lavery, T. J., Roudnew, B., Gill, P., Seymour, J., Seuront, L., Johnson, G., Mitchell, J. G., & Smetacek, V. (2010). Iron defecation by sperm whales stimulates carbon export in the Southern Ocean. Proceedings of the Royal Society B: Biological Sciences, 277(1699), 3527–3531. https://doi.org/10.1098/rspb.2010.0863
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Smith, C. R., Glover, A., Treude, T., Higgs, N. D., & Amon, D. (2015). Whale-fall ecosystems: Recent insights into ecology, paleoecology, and evolution. Annual Review of Marine Science. https://doi.org/10.1146/annurev-marine-010213-135144
Bik, E. M. et al. Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat. Commun. 7, 10516 (2016).