Cetacean microbiome

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The cetacean microbiome is the group of communities of microorganisms that reside within whales.

Contents

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

Gut

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

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 [10] and in many cases diatoms growing on the backs of migrating killer whales. [11]

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. [10] [12]

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 [12]

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. [13]

Respiratory system

Collection of blow from a blue whale using a radio-controlled helicopter Whale blow sampling with drone.png
Collection of blow from a blue whale using a radio-controlled helicopter
Relative abundance of taxonomic classes identified as whale-, air- or seawater-specific in each sample type. Cetacean blow's bacteria.png
Relative abundance of taxonomic classes identified as whale-, air- or seawater-specific in each sample type.
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. Viruses in cetacean.png
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.

Impact of cetacean respiratory system microbiome

The cetaceans are in danger because they are affected by multiple stress factors, especially anthropogenature, 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. The use of aerial drones has been more successful with large cetaceans due to slow swim speeds and larger blow sizes. [15] [17] [18] [19] [20] [14] [21] [22] [16]

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), [15] [17] [18] [16] Blue whale (Balænoptera musculus), [14] Gray whale (Eschrichtius robustus), [14] Sperm whale (Physeter macrocephalus), [14] Killer whale ( Orcinus orca) [21] and bottlenose dolphins (Tursiops truncatus), [19] [20] [22] 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 Pseudomonadota, Bacillota, Actinomycetota, and Bacteroidota.

Types of bacteria found in the respiratory systems of cetaceans

Among the Pseudomonadota, bacteria belonging to the families Brucellaceae and Enterobacteriaceae and to the genera "Candidatus Pelagibacter", Acidovorax , Cardiobacterium , Pseudomonas , Burkholderia , and Psychrobacter have been recognized.

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

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

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

To these are added bacteria belonging to the phylum Fusobacteriota and Mycoplasmatota.

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. [14]

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. [16]

Related Research Articles

<span class="mw-page-title-main">Human microbiome</span> Microorganisms in or on human skin and biofluids

The human microbiome is the aggregate of all microbiota that reside on or within human tissues and biofluids along with the corresponding anatomical sites in which they reside, including the gastrointestinal tract, skin, mammary glands, seminal fluid, uterus, ovarian follicles, lung, saliva, oral mucosa, conjunctiva, and the biliary tract. Types of human microbiota include bacteria, archaea, fungi, protists, and viruses. Though micro-animals can also live on the human body, they are typically excluded from this definition. In the context of genomics, the term human microbiome is sometimes used to refer to the collective genomes of resident microorganisms; however, the term human metagenome has the same meaning.

<span class="mw-page-title-main">Oceanic dolphin</span> Family of marine mammals

Oceanic dolphins or Delphinidae are a widely distributed family of dolphins that live in the sea. Close to forty extant species are recognised. They include several big species whose common names contain "whale" rather than "dolphin", such as the Globicephalinae. Delphinidae is a family within the superfamily Delphinoidea, which also includes the porpoises (Phocoenidae) and the Monodontidae. River dolphins are relatives of the Delphinoidea.

<span class="mw-page-title-main">Cetacean surfacing behaviour</span> Cetacean movement types

Cetacean surfacing behaviour is a grouping of movement types that cetaceans make at the water's surface in addition to breathing. Cetaceans have developed and use surface behaviours for many functions such as display, feeding and communication. All regularly observed members of the order Cetacea, including whales, dolphins and porpoises, show a range of surfacing behaviours.

<span class="mw-page-title-main">Gut microbiota</span> Community of microorganisms in the gut

Gut microbiota, gut microbiome, or gut flora are the microorganisms, including bacteria, archaea, fungi, and viruses, that live in the digestive tracts of animals. The gastrointestinal metagenome is the aggregate of all the genomes of the gut microbiota. The gut is the main location of the human microbiome. The gut microbiota has broad impacts, including effects on colonization, resistance to pathogens, maintaining the intestinal epithelium, metabolizing dietary and pharmaceutical compounds, controlling immune function, and even behavior through the gut–brain axis.

<span class="mw-page-title-main">Phyllosphere</span> The plant surface as a habitat for microorganisms

In microbiology, the phyllosphere is the total above-ground surface of a plant when viewed as a habitat for microorganisms. The phyllosphere can be further subdivided into the caulosphere (stems), phylloplane (leaves), anthosphere (flowers), and carposphere (fruits). The below-ground microbial habitats are referred to as the rhizosphere and laimosphere. Most plants host diverse communities of microorganisms including bacteria, fungi, archaea, and protists. Some are beneficial to the plant, while others function as plant pathogens and may damage the host plant or even kill it.

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Microecology means microbial ecology or ecology of a microhabitat. It is a large field that includes many topics such as: evolution, biodiversity, exobiology, ecology, bioremediation, recycling, and food microbiology. It can also refer to a hybrid urban network at the scale of the neighbourhood. It is the study of the interactions between living organisms and their environment, and how these interactions affect the organisms and their environment. Additionally, it is a multidisciplinary area of study, combining elements of biology, chemistry, physics, mathematics and urban planning. It focuses on the study of the interactions between microorganisms and the environment they inhabit, their effects on the environment, and their effects on other organisms. Microecology also studies the effects of human activity on the environment and how this affects the growth and development of microorganisms or organic structures. Microecology has many applications in the fields of medicine, agriculture, biotechnology and design. It is also important for understanding the cycling of nutrients in the environment, and the behavior of microorganisms or actors in various environments.

<span class="mw-page-title-main">Skin flora</span> Microbiota that reside on the skin

Skin flora, also called skin microbiota, refers to microbiota that reside on the skin, typically human skin.

<span class="mw-page-title-main">Human Microbiome Project</span> Former research initiative

The Human Microbiome Project (HMP) was a United States National Institutes of Health (NIH) research initiative to improve understanding of the microbiota involved in human health and disease. Launched in 2007, the first phase (HMP1) focused on identifying and characterizing human microbiota. The second phase, known as the Integrative Human Microbiome Project (iHMP) launched in 2014 with the aim of generating resources to characterize the microbiome and elucidating the roles of microbes in health and disease states. The program received $170 million in funding by the NIH Common Fund from 2007 to 2016.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, mutualistic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

A microbial consortium or microbial community, is two or more bacterial or microbial groups living symbiotically. Consortiums can be endosymbiotic or ectosymbiotic, or occasionally may be both. The protist Mixotricha paradoxa, itself an endosymbiont of the Mastotermes darwiniensis termite, is always found as a consortium of at least one endosymbiotic coccus, multiple ectosymbiotic species of flagellate or ciliate bacteria, and at least one species of helical Treponema bacteria that forms the basis of Mixotricha protists' locomotion.

<span class="mw-page-title-main">Human virome</span> Total collection of viruses in and on the human body

The human virome is the total collection of viruses in and on the human body. Viruses in the human body may infect both human cells and other microbes such as bacteria. Some viruses cause disease, while others may be asymptomatic. Certain viruses are also integrated into the human genome as proviruses or endogenous viral elements.

Parasutterella is a genus of Gram-negative, circular/rod-shaped, obligate anaerobic, non-spore forming bacteria from the Pseudomonadota phylum, Betaproteobacteria class and the family Sutterellaceae. Previously, this genus was considered "unculturable," meaning that it could not be characterized through conventional laboratory techniques, such as grow in culture due its unique requirements of anaerobic environment. The genus was initially discovered through 16S rRNA sequencing and bioinformatics analysis. By analyzing the sequence similarity, Parasutterella was determined to be related most closely to the genus Sutterella and previously classified in the family Alcaligenaceae.

<i>Brucella ceti</i> Species of bacterium

Brucella ceti is a gram negative bacterial pathogen of the Brucellaceae family that causes brucellosis in cetaceans. Brucella ceti has been found in both classes of cetaceans, mysticetes and odontocetes. Brucellosis in some dolphins and porpoises can result in serious clinical signs including fetal abortions, male infertility, neurobrucellosis, cardiopathies, bone and skin lesions, stranding events, and death.

<span class="mw-page-title-main">Microbiome</span> Microbial community assemblage and activity

A microbiome is the community of microorganisms that can usually be found living together in any given habitat. It was defined more precisely in 1988 by Whipps et al. as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity". In 2020, an international panel of experts published the outcome of their discussions on the definition of the microbiome. They proposed a definition of the microbiome based on a revival of the "compact, clear, and comprehensive description of the term" as originally provided by Whipps et al., but supplemented with two explanatory paragraphs, the first pronouncing the dynamic character of the microbiome, and the second clearly separating the term microbiota from the term microbiome.

<span class="mw-page-title-main">Pharmacomicrobiomics</span>

Pharmacomicrobiomics, proposed by Prof. Marco Candela for the ERC-2009-StG project call, and publicly coined for the first time in 2010 by Rizkallah et al., is defined as the effect of microbiome variations on drug disposition, action, and toxicity. Pharmacomicrobiomics is concerned with the interaction between xenobiotics, or foreign compounds, and the gut microbiome. It is estimated that over 100 trillion prokaryotes representing more than 1000 species reside in the gut. Within the gut, microbes help modulate developmental, immunological and nutrition host functions. The aggregate genome of microbes extends the metabolic capabilities of humans, allowing them to capture nutrients from diverse sources. Namely, through the secretion of enzymes that assist in the metabolism of chemicals foreign to the body, modification of liver and intestinal enzymes, and modulation of the expression of human metabolic genes, microbes can significantly impact the ingestion of xenobiotics.

<span class="mw-page-title-main">Human milk microbiome</span> Community of microorganisms in human milk

The human milk microbiota, also known as human milk probiotics (HMP), encompasses the microbiota–the community of microorganisms–present within the human mammary glands and breast milk. Contrary to the traditional belief that human breast milk is sterile, advancements in both microbial culture and culture-independent methods have confirmed that human milk harbors diverse communities of bacteria. These communities are distinct in composition from other microbial populations found within the human body which constitute the human microbiome.

<span class="mw-page-title-main">Marine microbiome</span>

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.

The poultry microbiome is an understudied, yet extremely impactful part of the poultry industry. Poultry is defined as any avian species used for production purposes such as food or down feathers. The United States consumes more poultry, specifically broiler meat, than any other type of protein. Worldwide, poultry makes up 33% of consumed meat. This makes poultry extremely valuable and the impact of the poultry microbiome on health and production even more valuable. Antonie van Leeuwenhoek was the first to notice microbes inside animals through stool samples giving light to further research into the gut microbiome. His discovery lead to the ever evolving study of the microbiota and microbiome. The microbiota is the entirety of living organisms including bacteria, viruses, fungi, and archaea in an environment. The microbiome is the combination of the microbiota and the additional activities in that system including metabolites and chemicals in a habitat. Much of the work done to characterize the poultry microbiome has been accomplished over the past decade and was done through the use of 16s rRNA sequencing.

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