Hologenomics

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Hologenomics is the omics study of hologenomes. A hologenome is the whole set of genomes of a holobiont, an organism together with all co-habitating microbes, other life forms, and viruses. [1] While the term hologenome originated from the hologenome theory of evolution, which postulates that natural selection occurs on the holobiont level, [2] hologenomics uses an integrative framework to investigate interactions between the host and its associated species. Examples include gut microbe [3] or viral [4] genomes linked to human or animal genomes for host-microbe interaction research. [5] Hologenomics approaches have also been used to explain genetic diversity in the microbial communities of marine sponges. [6]

Contents

History

The origins of hologenomics revolves around the hologenome theory of evolution, which describes individual multicellular organisms, microbes, and viruses establishing symbiotic relationships and undergoing coevolution together. [2] [7] Richard Jefferson introduced the term 'hologenome' to describe the host-symbiont genome as an evolutionary unit. [8] Prior to this, Lynn Margulis used the term 'holobiont' to describe hosts and their associated species as an ecological unit. [9]

Eukaryotes-prokaryotes coevolution

Distinct microbial communities in sponges converge to have common functionality despite retaining phylogenetic differences. The sponge hologenome.jpg
Distinct microbial communities in sponges converge to have common functionality despite retaining phylogenetic differences.

Earliest evidence of multicellular-unicellular interactions are seen in sponges, which are a well studied hologenomic system. Porifera are often described as holobionts because they harbor a wide range of bacteria, archaea and algae. Microbial communities present have been observed in facilitating metabolic functions and immune responses. [10] Offspring inherit these microbial colonies via vertical and/or horizontal transmission. [10] Symbiont colonies are transferred through parental gametes in vertical transmission, whereas offspring acquire same colonies from their environment in horizontal transmission. Vertical transmission is also seen in terrestrial organisms like C. ocellatus , where gammaproteobacteria in the parental gut is vertically transferred through egg contamination. [11]

Criticism

The hologenome theory evolution is not fully accepted, and research in microbial-host phylogenetics is ongoing. Rather than the selection of corals with certain symbiotic microbial communities, coral bleaching may simply be a result of environmental stressors, and bacterial presence in bleached coral may be explained simply as opportunistic colonization. [12] Ubiquity testing also revealed many different bacterial and algal symbionts that are not associated with a single species of coral, [13] suggesting that hologenomics just identifies and validates mechanistic interactions between pathogens, microbes, and their hosts. [14]

Examples of discoveries with hologenomic approaches

Applications

Medicine

It's hypothesized the continued incidence non-infectious diseases is a result of modernization reducing the diversity of symbiotic microbes. [14] The human microbiome has also been correlated to numerous etiologies of non-communicable disease, such as brain disorders, [18] cancer, [19] [20] and heart disease. [21] Interactions between human microbiome and human health are complex and suggest a hologenomic approach.

Disease biomarkers can be found by investigating lifestyle, genomic differences, and mRNA/protein/metabolite profiles of the patient and their microbiota. [14] For investigating microbiomes and specifically microbiota subcommunities that may contribute to a disease phenotype, longitudinal studies are recommended as everyone has a personalized microbiome with small differences in microbiome phylotypes. [14] A personalized plan managing a person’s microbiome can then be developed, with prebiotics nurturing beneficial endogenous microbes, and probiotics manipulating a person’s hologenome. [22]

Immunology

Conditional mutualism, where parasites have mutualistic effects under certain environmental/ecological conditions, have been found with holobiont-holobiont interactions. [23] Maturation of mammalian host immune systems has been known to involve gastrointestinal flora. [24] Understanding microorganism recognition of foreign pathogenic invasion and how host immunity favors the most ideal symbiont may aid in discovering novel therapeutic treatments to combat evolving diseases.

See also

Related Research Articles

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.

<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 skin, mammary glands, seminal fluid, uterus, ovarian follicles, lung, saliva, oral mucosa, conjunctiva, biliary tract, and gastrointestinal 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.

Joan Roughgarden is an American ecologist and evolutionary biologist. She has engaged in theory and observation of coevolution and competition in Anolis lizards of the Caribbean, and recruitment limitation in the rocky intertidal zones of California and Oregon. She has more recently become known for her rejection of sexual selection, her theistic evolutionism, and her work on holobiont evolution.

Symbiotic bacteria are bacteria living in symbiosis with another organism or each other. For example, rhizobia living in root nodules of legumes provide nitrogen fixing activity for these plants.

<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.

For the American folk-rock singer-songwriter, see Nancy Moran.

The hologenome theory of evolution recasts the individual animal or plant as a community or a "holobiont" – the host plus all of its symbiotic microbes. Consequently, the collective genomes of the holobiont form a "hologenome". Holobionts and hologenomes are structural entities that replace misnomers in the context of host-microbiota symbioses such as superorganism, organ, and metagenome. Variation in the hologenome may encode phenotypic plasticity of the holobiont and can be subject to evolutionary changes caused by selection and drift, if portions of the hologenome are transmitted between generations with reasonable fidelity. One of the important outcomes of recasting the individual as a holobiont subject to evolutionary forces is that genetic variation in the hologenome can be brought about by changes in the host genome and also by changes in the microbiome, including new acquisitions of microbes, horizontal gene transfers, and changes in microbial abundance within hosts. Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts. For recent literature on holobionts and hologenomes published in an open access platform, see the following reference.

<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 explanatory paragraph pronounces the dynamic character of the microbiome, and the second explanatory paragraph clearly separates the term microbiota from the term microbiome.

Metatranscriptomics is the set of techniques used to study gene expression of microbes within natural environments, i.e., the metatranscriptome.

<span class="mw-page-title-main">Poribacteria</span> Phylum of bacteria

Poribacteria are a candidate phylum of bacteria originally discovered in the microbiome of marine sponges (Porifera). Poribacteria are Gram-negative primarily aerobic mixotrophs with the ability for oxidative phosphorylation, glycolysis, and autotrophic carbon fixation via the Wood – Ljungdahl pathway. Poribacterial heterotrophy is characterised by an enriched set of glycoside hydrolases, uronic acid degradation, as well as several specific sulfatases. This heterotrophic repertoire of poribacteria was suggested to be involved in the degradation of the extracellular sponge host matrix.

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

Microbial symbiosis in marine animals was not discovered until 1981. In the time following, symbiotic relationships between marine invertebrates and chemoautotrophic bacteria have been found in a variety of ecosystems, ranging from shallow coastal waters to deep-sea hydrothermal vents. Symbiosis is a way for marine organisms to find creative ways to survive in a very dynamic environment. They are different in relation to how dependent the organisms are on each other or how they are associated. It is also considered a selective force behind evolution in some scientific aspects. The symbiotic relationships of organisms has the ability to change behavior, morphology and metabolic pathways. With increased recognition and research, new terminology also arises, such as holobiont, which the relationship between a host and its symbionts as one grouping. Many scientists will look at the hologenome, which is the combined genetic information of the host and its symbionts. These terms are more commonly used to describe microbial symbionts.

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

Eugene Rosenberg is a microbiologist at the Faculty of Life Sciences at Tel Aviv University, an expert in the field of applied environmental microbiology, in particular his work on Myxobacteria, microorganisms to combat pollution (bioremediation), and the Hologenome theory of evolution.

<span class="mw-page-title-main">Mycobiome</span> The fungal community in and on an organism

The mycobiome, mycobiota, or fungal microbiome, is the fungal community in and on an organism.

<span class="mw-page-title-main">Holobiont</span> Host and associated species living as a discrete ecological unit

A holobiont is an assemblage of a host and the many other species living in or around it, which together form a discrete ecological unit through symbiosis, though there is controversy over this discreteness. The components of a holobiont are individual species or bionts, while the combined genome of all bionts is the hologenome. The holobiont concept was initially introduced by the German theoretical biologist Adolf Meyer-Abich in 1943, and then apparently independently by Dr. Lynn Margulis in her 1991 book Symbiosis as a Source of Evolutionary Innovation. The concept has evolved since the original formulations. Holobionts include the host, virome, microbiome, and any other organisms which contribute in some way to the functioning of the whole. Well-studied holobionts include reef-building corals and humans.

Endozoicomonas is a genus of Gram-negative, aerobic or facultatively anaerobic, chemoorganotrophic, rod-shaped, marine bacteria from the family of Endozoicomonadaceae. Endozoicomonas are symbionts of marine animals.

Vertical transmission of symbionts is the transfer of a microbial symbiont from the parent directly to the offspring. Many metazoan species carry symbiotic bacteria which play a mutualistic, commensal, or parasitic role. A symbiont is acquired by a host via horizontal, vertical, or mixed transmission.

<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.

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

The plant microbiome, also known as the phytomicrobiome, plays roles in plant health and productivity and has received significant attention in recent years. The microbiome has been defined 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".

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

Since the colonization of land by ancestral plant lineages 450 million years ago, plants and their associated microbes have been interacting with each other, forming an assemblage of species that is often referred to as a holobiont. Selective pressure acting on holobiont components has likely shaped plant-associated microbial communities and selected for host-adapted microorganisms that impact plant fitness. However, the high microbial densities detected on plant tissues, together with the fast generation time of microbes and their more ancient origin compared to their host, suggest that microbe-microbe interactions are also important selective forces sculpting complex microbial assemblages in the phyllosphere, rhizosphere, and plant endosphere compartments.

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

The holobiont concept is a renewed paradigm in biology that can help to describe and understand complex systems, like the host-microbe interactions that play crucial roles in marine ecosystems. However, there is still little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them and their ecological consequences. The holobiont concept posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution.

References

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