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Microbiome refers to different communities of microorganisms and their role within a specific environment, considering environmental conditions and interactions with one another in a defined environment. A defined environment could be an entire organism (e.g., a human being) or parts of it (e.g., the gut or the skin).

Microbiomes play an important role in individual health and ecology and in particular in marine mammals the discovery of different microbiomes in gut, skin and nose permitted to analyze their conditions and the condition of the marine environment in which they live.

Gut Microbiome

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The access of microbial samples from the gut out of marine mammals is limited because most species are rare, endangered, and deep divers. There are different techniques for sampling the cetacean's gut microbiome. The most common is collecting fecal samples from the environment and taking a probe from the center that is non-contaminated.[1] Besides there are studies from rectal swabs and rare studies from stranded dead or living animals direct from the intestine.[2] [3] [4]

The intestinal microbiome of Cetaceans is a complex ecosystem that plays an important role in the metabolism, health, and immunity of the host.[5] The microbial communities of marine mammals are diverse and distinct from terrestrial mammals, and the community depends on different factors like kind of diet, phylogeny, health, and age.[3]

As the microbiome is involved in the decomposition of food, diet is a predominant factor for the microbial community. Different studies have shown that members of Bacteroidetes and Firmicutes are the most abundant phyla of gut microorganisms in animals that are cephalopod predators or zooplankton predators like in short-finned pilot whales and baleen whales.[4][6] Especially the genus Bacteroides (phyla Bacteroidetes) seems to play a major role in the decomposition of the chitin-rich diet of these species and were also found in the gut microbiome of baleen whales.[6]

In toothed cetacean species which food consumption is mainly piscivore the most abundant phyla are Firmicutes, Fusobacteria, and Proteobacteria.[7] Proteobacteria are classified as a minor important group for marine mammals that consume cephalopods and zooplankton but are highly abundant in piscivorous predators like bottlenose dolphins, East Asian finless porpoises, and belugas. These findings could mirror the different dietary niches of these species.[8]

Besides the dietary also the age seems to determine the differences in the microbial community between cetaceans. Maron et al. have shown that the microbial community is changing in right whale caves during their development. Interestingly the genera Bilophila, Peptococcus, and Treponema are more abundant in older calves. The higher abundance of Bilophila might be a response to the greater milk intake of the older calves.[9]

Skin Microbiome

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the outermost epidermal layer, i.e. the skin, is the first barrier that protects the individual from the outside world and the epidermal microbiome on it is considered an indicator not only of the health of the animal but is also considered an ecological indicator that shows the state of the surrounding environment. Knowing the microbiome of the skin of marine mammals under ''normal'' conditions has allowed us to understand how these communities are different from the free microbial communities found in the sea and how they can change according to abiotic and biotic variations, and also ''communities vary between healthy and sick individuals'' [10]

Different studies on migratory marine mammals in particular Megaptera novaeangliae, killer whales, Orcinus orca, and Beluga whales, which are exposed to different habitats host different communities of Bacterioplankton [11] and in many cases diatoms growing on the backs of migrating killer whales.[12]

Although studies on the microbiome of the skin of these marine mammals are quite limited, thanks to the amplification of SSU rRNA genes, were discovered communities belonging to the phylum Bacteroidetes, in particular of the family Flavobacteriaceae, the genus Tenacibaculum dicentrarchi, and it seems that the role of these bacteria is to regulate the microbiome present on the skin of marine mammals, acting as predators and limit the exponential growth of other communities.[13][14]

Another type of bacterium found on the skin of cetaceans is Phychrobacter, able to tolerate low temperatures and therefore present during migratory routes to high latitudes, it was also discovered that this bacterium is one of those controlled by T. dicentrarchi; while in skin lesions the bacterium spp. Moraxella was found, but not only also in healthy skin such as blowholes and mouths of dolphins [15]

It is not well known whether these communities of microorganisms are transient colonizers of the skin surface or have adapted to that environment, thus subjecting themselves to variations in extrinsic and intrinsic factors that go to change the communities of the skin microbiome, such as UV rays, skin detachment, which seems to be involved in the change of the microbial communities, the change of pressure and temperature, which influences a regional and temporal variability of the skin microbiome, the sex, the age and the health status of the individual, all influence the microbiome and the change of the skin communities. In conjunction with these factors, climate change has been shown to further influence the growth and presence of certain bacterial communities as well as the health status of these cetaceans. [16]

The microbiome of the respiratory system

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Photograph showing the collection of blow from a blue whale Balaenoptera musculus using a radio-controlled helicopter[17]

The cetaceans are in danger because they are affected by multiple stress factors, especially of an anthropogenic nature, which make them more vulnerable to various diseases. These animals have been noted to show high susceptibility to airway infections, but very little is known about their respiratory microbiome. Therefore, the sampling of the exhaled breath or "blow" of the cetaceans can provide an assessment of the state of health. Blow is composed of a mixture of microorganisms and organic material, including lipids, proteins and cellular debris derived from the linings of the airways which, when released into the relatively cooler outdoor air, condense to form a visible mass of vapor, which can be collected. There are various methods for collecting exhaled breath samples, one of the most recent is through the use of aerial drones. This method provides a safer, quieter, and less invasive alternative and often a cost-effective option for monitoring fauna and flora. Once obtained, the blow samples are taken to the laboratory and we proceed with the amplification and sequencing of the respiratory tract microbiota. The use of aerial drones has been more successful with large cetaceans due to slow swim speeds and larger blow sizes.[18][19][20][21][22][17][23][24][25]

In all the studies carried out, in addition to exhaled breath samples, seawater and air samples were collected to more accurately identify the specific microorganisms for exhaled breath.

Through various studies carried out on different cetaceans, among which, Humpback whales (Megaptera novaeangliae)[18][19] [20][25], Blue whale (Balænoptera musculus) [17], Gray whale (Eschrichtius robustus) [17], Sperm whale (Physeter macrocephalus) [17], Killer whale ( Orcinus orca) [23] and bottlenose dolphins (Tursiops truncatus)[21][22][24], the respiratory microbiome has begun to be defined, i.e., a microbial community formed by a complex diversity of common microorganisms to all the specimens examined. These are very recent studies, so knowledge is very limited, only some microorganisms are known while others have not yet been identified and little is known about their functional role within these animals. Overall, the most common bacteria identified at the phylum level included Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes.

Among the Proteobacteria, bacteria belonging to the families Brucellaceae and Enterobacteriaceae and to the genera Candidatus Pelagibacter, Acidovorax, Cardiobacterium, Pseudomonas, Burkholderia, Psychrobacter and some Deltaproteobacteria and Epsilonproteobacteria have been recognized.

Among the Firmicutes, bacteria belonging to the Clostridia and Erysipelotrichia classes and to the genera Anoxybacillus, Paenibacillus and Leptotrichia have been recognized.

Relative abundance of taxonomic classes identified as whale-, air- or seawater-specific in each sample type[18].

Bacteria belonging to the Acidimicrobiia class, to the Microbacteriaceae family, and to the genera Corynebacterium, Mycobacterium and Propionibacterium (Cutibacterium), have been recognized among the Actinobacteria

Among the Bacteroidetes, bacteria belonging to the genus Tenacibaculum have been recognized.

To these are added bacteria belonging to the phylum Fusobacteria and Mollicutes.

Finally, potential respiratory pathogens were also detected, such as Balneatrix (proteobacteria) and a range of Gram-positive Clostridia and Bacilli, such as Staphylococcus and Streptococcus (both firmicutes).

Furthermore, one of the most common bacteria in the various cetacean species is the Haemophilus bacterium. These are opportunistic gram-negative coccobacilli, also found in the respiratory tract of humans and other animals, which tend to colonize but without causing the onset of infection. But during periods of immunosuppression these organisms can cause damage by generating meningitis and pneumonia.[17]

Some samples of killer whale blows were subjected to sensitivity tests, which revealed the presence of both gram-positive and gram-negative bacteria resistant to multiple antibodies such as erythromycin, lincomycin, penicillin and ampicillin.[23]

In addition to bacteria, some viruses have also been identified in whale exhaled breath. Among the most abundant bacteriophages were the Siphoviridae and Myoviridae, while among the viral families there were small single-stranded DNA viruses (ss), in particular the Circoviridae, members of the Parvoviridae and a family of RNA viruses, the Tombusviridae.[25]

Relative abundance of viruses and their taxonomic families. This included 42 viral families, including 29 families of bacteriophage. Percentages indicate relative abundance of all viruses in the sequence library[25].

To conclude the persistence of these central members, which make up the respiratory microbiome, in apparently healthy individuals suggests that they may be indicative of a healthy, uninfected lung system, and their presence or absence could be informative for cetacean health monitoring. In fact, in exhaled breath samples, of some specimens, a low number of cores and a lower biodiversity than that previously listed were found. An explanation for this phenomenon could be that the samples in question were collected from animals following migration and therefore the depletion of the microbiota may reflect a compromised state of health due to the consequences of migration.[20]

References

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  1. ^ Suzuki A, Ueda K, Segawa T, Suzuki M. 2019. Fecal microbiota of captive Antillean manatee Trichechus manatus manatus. FEMS Microbiology Letters 366.
  2. ^ Sehnal L, Brammer-Robbins E, Wormington AM, Blaha L, Bisesi J, Larkin I, Martyniuk CJ, Simonin M, Adamovsky O. 2021. Microbiome Composition and Function in Aquatic Vertebrates: Small Organisms Making Big Impacts on Aquatic Animal Health. Frontiers in Microbiology 12.
  3. ^ a b Bik EM, Costello EK, Switzer AD, Callahan BJ, Holmes SP, Wells RS, Carlin KP, Jensen ED, Venn-Watson S, Relman DA. 2016. Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nature Communications 7:10516.
  4. ^ a b 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 16:324–335.
  5. ^ Liu Z, Li A, Wang Y, Iqbal M, Zheng A, Zhao M, Li Z, Wang N, Wu C, Yu D. 2020. Comparative analysis of microbial community structure between healthy and Aeromonas veronii-infected Yangtze finless porpoise. Microbial Cell Factories 19:123.
  6. ^ a b Sanders JG, Beichman AC, Roman J, Scott JJ, Emerson D, McCarthy JJ, Girguis PR. 2015. Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nature Communications 6:8285.
  7. ^ WAN X, LI J, CHENG Z, AO M, TIAN R, MCLAUGHLIN RW, ZHENG J, WANG D. 2021. The intestinal microbiome of an Indo‐Pacific humpback dolphin ( Sousa chinensis ) stranded near the Pearl River Estuary, China. Integrative Zoology 16:287–299.
  8. ^ Wan X-L, McLaughlin RW, 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 8:14142.
  9. ^ Marón CF, Kohl KD, Chirife A, di Martino M, Fons MP, Navarro MA, Beingesser J, McAloose D, Uzal FA, Dearing MD, Rowntree VJ, Uhart M. 2019. Symbiotic microbes and potential
  10. ^ Apprill, Amy; Mooney, T. Aran; Lyman, Edward; Stimpert, Alison K.; Rappé, Michael S. (2011). "Humpback whales harbour a combination of specific and variable skin bacteria". Environmental Microbiology Reports. 3 (2): 223–232. doi:10.1111/j.1758-2229.2010.00213.x. ISSN 1758-2229.
  11. ^ Apprill, Amy; Mooney, T. Aran; Lyman, Edward; Stimpert, Alison K.; Rappé, Michael S. (2011). "Humpback whales harbour a combination of specific and variable skin bacteria". Environmental Microbiology Reports. 3 (2): 223–232. doi:10.1111/j.1758-2229.2010.00213.x. ISSN 1758-2229.
  12. ^ Hooper, Rebecca; Brealey, Jaelle C.; Valk, Tom van der; Alberdi, Antton; Durban, John W.; Fearnbach, Holly; Robertson, Kelly M.; Baird, Robin W.; Hanson, M. Bradley; Wade, Paul; Gilbert, M. Thomas P. (2019). "Host-derived population genomics data provides insights into bacterial and diatom composition of the killer whale skin". Molecular Ecology. 28 (2): 484–502. doi:10.1111/mec.14860. ISSN 1365-294X. PMC 6487819. PMID 30187987.{{cite journal}}: CS1 maint: PMC format (link)
  13. ^ Apprill, Amy; Mooney, T. Aran; Lyman, Edward; Stimpert, Alison K.; Rappé, Michael S. (2011). "Humpback whales harbour a combination of specific and variable skin bacteria". Environmental Microbiology Reports. 3 (2): 223–232. doi:10.1111/j.1758-2229.2010.00213.x. ISSN 1758-2229.
  14. ^ Bierlich, K. C.; Miller, Carolyn; DeForce, Emelia; Friedlaender, Ari S.; Johnston, David W.; Apprill, Amy (2017-12-21). "Temporal and Regional Variability in the Skin Microbiome of Humpback Whales along the Western Antarctic Peninsula". Applied and Environmental Microbiology. doi:10.1128/AEM.02574-17. PMC 5812929. PMID 29269499.{{cite journal}}: CS1 maint: PMC format (link)
  15. ^ Bierlich, K. C.; Miller, Carolyn; DeForce, Emelia; Friedlaender, Ari S.; Johnston, David W.; Apprill, Amy (2017-12-21). "Temporal and Regional Variability in the Skin Microbiome of Humpback Whales along the Western Antarctic Peninsula". Applied and Environmental Microbiology. doi:10.1128/AEM.02574-17. PMC 5812929. PMID 29269499.{{cite journal}}: CS1 maint: PMC format (link)
  16. ^ "GEOGRAPHIC INFLUENCES ON THE SKIN MICROBIOME OF HUMPBACK WHALES" (PDF). GEOGRAPHIC INFLUENCES ON THE SKIN MICROBIOME OF HUMPBACK WHALES. {{cite journal}}: horizontal tab character in |journal= at position 11 (help); horizontal tab character in |title= at position 11 (help)
  17. ^ a b c d e f Acevedo-Whitehouse, K.; Rocha-Gosselin, A.; Gendron, D. (2010). "A novel non-invasive tool for disease surveillance of free-ranging whales and its relevance to conservation programs". Animal Conservation. 13 (2): 217–225. doi:10.1111/j.1469-1795.2009.00326.x. ISSN 1469-1795. Cite error: The named reference ":5" was defined multiple times with different content (see the help page).
  18. ^ a b c Pirotta V, Smith A, Ostrowski M, Russell D, Jonsen ID, Grech A and Harcourt R (2017) An Economical Custom-Built Drone for Assessing Whale Health. Front. Mar. Sci. 4:425. doi: 10.3389/fmars.2017.00425
  19. ^ a b Apprill, Amy & Miller, Carolyn & Moore, Michael & Durban, John & Fearnbach, Holly & Barrett-Lennard, Lance. (2017). Extensive Core Microbiome in Drone-Captured Whale Blow Supports a Framework for Health Monitoring. mSystems. 2. e00119-17. 10.1128/mSystems.00119-17.
  20. ^ a b c C Vendl, B C Ferrari, T Thomas, E Slavich, E Zhang, T Nelson, T Rogers, Interannual comparison of core taxa and community composition of the blow microbiota from East Australian humpback whales, FEMS Microbiology Ecology, Volume 95, Issue 8, August 2019, fiz102,
  21. ^ a b Johnson WR, Torralba M, Fair PA, Bossart GD, Nelson KE, Morris PJ. Novel diversity of bacterial communities associated with bottlenose dolphin upper respiratory tracts. Environ Microbiol Rep. 2009 Dec;1(6):555-62. doi: 10.1111/j.1758-2229.2009.00080.x. Epub 2009 Oct 2. PMID: 23765934.
  22. ^ a b Centelleghe C, Carraro L, Gonzalvo J, Rosso M, Esposti E, Gili C, Bonato M, Pedrotti D, Cardazzo B, Povinelli M, Mazzariol S. The use of Unmanned Aerial Vehicles (UAVs) to sample the blow microbiome of small cetaceans. PLoS One. 2020 Jul 2;15(7):e0235537. doi: 10.1371/journal.pone.0235537. Erratum in: PLoS One. 2021 Jan 22;16(1):e0246177. PMID: 32614926; PMCID: PMC7332044.
  23. ^ a b c Raverty, S.A., Rhodes, L.D., Zabek, E. et al. Respiratory Microbiome of Endangered Southern Resident Killer Whales and Microbiota of Surrounding Sea Surface Microlayer in the Eastern North Pacific. Sci Rep 7, 394 (2017). https://doi.org/10.1038/s41598-017-00457-5
  24. ^ a b Lima N, Rogers T, Acevedo-Whitehouse K, Brown MV. Temporal stability and species specificity in bacteria associated with the bottlenose dolphins respiratory system. Environ Microbiol Rep. 2012 Feb;4(1):89-96. doi: 10.1111/j.1758-2229.2011.00306.x. Epub 2011 Nov 27. PMID: 23757234.
  25. ^ a b c d Geoghegan, J.L.; Pirotta, V.; Harvey, E.; Smith, A.; Buchmann, J.P.; Ostrowski, M.; Eden, J.-S.; Harcourt, R.; Holmes, E.C. Virological Sampling of Inaccessible Wildlife with Drones. Viruses 2018, 10, 300. https://doi.org/10.3390/v10060300

Category:Microbiology Category:Cetaceans

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