Microbiome

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''. Modified text was copied from this source, which is available under
Creative Commons Attribution 4.0 International License

The microbiota consists of all living members forming the microbiome. Most microbiome researchers agree bacteria, archaea, fungi, algae, and small protists should be considered as members of the microbiome. The integration of phages, viruses, plasmids, and mobile genetic elements is more controversial. Whipps's "theatre of activity" includes the essential role secondary metabolites play in mediating complex interspecies interactions and ensuring survival in competitive environments. Quorum sensing induced by small molecules allows bacteria to control cooperative activities and adapts their phenotypes to the biotic environment, resulting, e.g., in cell–cell adhesion or biofilm formation.

All animals and plants 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 microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and the multi-member microbiome. The potential for microbiomes to influence the health, physiology, behaviour, and ecology of marine animals could alter current understandings of how marine animals adapt to change. This applies to especially the growing climate-related and anthropogenic-induced changes already impacting the ocean and the phytoplankton microbiome in it. The plant microbiome plays key roles in plant health and food production and has received significant attention in recent years. Plants live in association with diverse microbial consortia, referred to as the plant microbiota, living both inside (the endosphere) and outside (the episphere) plant tissues. They play important roles in the ecology and physiology of plants. The core plant microbiome is thought to contain keystone microbial taxa essential for plant health and for the fitness of the plant holobiont. Likewise, the mammalian gut microbiome has emerged as a key regulator of host physiology, and coevolution between host and microbial lineages has played a key role in the adaptation of mammals to their diverse lifestyles.

Microbiome research originated in microbiology in the seventeenth century. The development of new techniques and equipment boosted microbiological research and caused paradigm shifts in understanding health and disease. The development of the first microscopes allowed the discovery of a new, unknown world and led to the identification of microorganisms. Infectious diseases became the earliest focus of interest and research. However, only a small proportion of microorganisms are associated with disease or pathogenicity. The overwhelming majority of microbes are essential for healthy ecosystem functioning and are known for beneficial interactions with other microbes and organisms. The concept that microorganisms exist as single cells began to change as it became increasingly obvious that microbes occur within complex assemblages in which species interactions and communication are critical. Discovery of DNA, the development of sequencing technologies, PCR, and cloning techniques enabled the investigation of microbial communities using cultivation-independent approaches. Further paradigm shifts occurred at the beginning of this century and still continue, as new sequencing technologies and accumulated sequence data have highlighted both the ubiquity of microbial communities in association within higher organisms and the critical roles of microbes in human, animal, and plant health. These have revolutionised microbial ecology. The analysis of genomes and metagenomes in a high-throughput manner now provides highly effective methods for researching the functioning of individual microorganisms as well as whole microbial communities in natural habitats.

Background

History

Microbiome research originated in microbiology and started back in the seventeenth century. The development of new techniques and equipment has boosted microbiological research and caused paradigm shifts in understanding health and disease. Since infectious diseases have affected human populations throughout most of history, medical microbiology was the earliest focus of research and public interest. Additionally, food microbiology is an old field of empirical applications. The development of the first microscopes allowed the discovery of a new, unknown world and led to the identification of microorganisms.

File:Microbiome paradigm shifts.png, Shift of paradigm from microbes as unsocial organisms causing diseases to a holistic view of microorganisms as the centre of the One Health Concept interconnecting all areas of human lives.

Access to the previously invisible world opened the eyes and the minds of the researchers of the seventeenth century. Antonie van Leeuwenhoek investigated diverse bacteria of various shapes, fungi, and protozoa, which he called animalcules, mainly from water, mud, and dental plaque samples, and discovered biofilms as a first indication of microorganisms interacting within complex communities. Robert Koch's explanation of the origin of human and animal diseases as a consequence of microbial infection and development of the concept of pathogenicity was an important milestone in microbiology. These findings shifted the focus of the research community and the public on the role of microorganisms as disease-forming agents that needed to be eliminated.

However, comprehensive research over the past century has shown only a small proportion of microorganisms are associated with disease or pathogenicity. The overwhelming majority of microbes are essential for ecosystem functioning and known for beneficial interactions with other microbes as well as macroorganisms. In fact, maintaining a healthy microbiome is essential for human health and may be a target for new therapeutics. At the end of the nineteenth century, microbial ecology started with the pioneering work by Martinus W. Beijerinck and Sergei Winogradsky. The newly established science of environmental microbiology resulted in another paradigm shift: microorganisms are everywhere in natural environments, often associated with hosts and, for the first time, beneficial effects on their hosts were reported.

Subsequently, the concept that microorganisms exist as single cells began to change as it became increasingly obvious that microbes occur within complex assemblages in which species interactions and communication are critical to population dynamics and functional activities. Discovery of DNA, the development of sequencing technologies, PCR, and cloning techniques enabled the investigation of microbial communities using cultivation-independent, DNA and RNA-based approaches.

A further important step was the introduction of phylogenetic markers such as the 16S rRNA gene for microbial community analysis by Carl Woese and George E. Fox in 1977. Nowadays biologists can barcode bacteria, archaea, fungi, algae, and protists in their natural habitats, e.g., by targeting their 16S and 18S rRNA genes, internal transcribed spacer (ITS), or, alternatively, specific functional regions of genes coding for specific enzymes.

Another major paradigm shift was initiated at the beginning of this century and continues through today, as new sequencing technologies and accumulated sequence data have highlighted both the ubiquity of microbial communities in association within higher organisms and the critical roles of microbes in human, animal, and plant health. These new possibilities have revolutionized microbial ecology, because the analysis of genomes and metagenomes in a high-throughput manner provides efficient methods for addressing the functional potential of individual microorganisms as well as of whole communities in their natural habitats. Multiomics technologies including metatranscriptome, metaproteome and metabolome approaches now provide detailed information on microbial activities in the environment. Based on the rich foundation of data, the cultivation of microbes, which was often ignored or underestimated over the last thirty years, has gained new importance, and high throughput culturomics is now an important part of the toolbox to study microbiomes. The high potential and power of combining multiple "omics" techniques to analyze host-microbe interactions are highlighted in several reviews.

Etymology

The word microbiome (from the Greek ''micro'' meaning "small" and ''bíos'' meaning "life") was first used by J.L. Mohr in 1952 in The Scientific Monthly to mean the microorganisms found in a specific environment.

Definitions

Microbial communities have commonly been defined as the collection of microorganisms living together. More specifically, microbial communities are defined as multi-species assemblages, in which (micro) organisms interact with each other in a contiguous environment. In 1988, Whipps and colleagues working on the ecology of rhizosphere microorganisms provided the first definition of the term microbiome. They described the microbiome as a combination of the words ''micro'' and ''biome'', naming a "characteristic microbial community" in a "reasonably well-defined habitat which has distinct physio-chemical properties" as their "theatre of activity". This definition represents a substantial advancement of the definition of a microbial community, as it defines a microbial community with distinct properties and functions and its interactions with its environment, resulting in the formation of specific ecological niches.

However, many other microbiome definitions have been published in recent decades. By 2020 the most cited definition was by Lederberg, and described microbiomes within an ecological context as a community of commensal, symbiotic, and pathogenic microorganisms within a body space or other environment. Marchesi and Ravel focused in their definition on the genomes and microbial (and viral) gene expression patterns and proteomes in a given environment and its prevailing biotic and abiotic conditions. All these definitions imply that general concepts of macro-ecology could be easily applied to microbe-microbe as well as to microbe-host interactions. However, the extent to which these concepts, developed for macro-eukaryotes, can be applied to prokaryotes with their different lifestyles regarding dormancy, variation of phenotype, and horizontal gene transfer as well as to micro-eukaryotes that is not quite clear. This raises the challenge of considering an entirely novel body of conceptual ecology models and theory for microbiome ecology, particularly in relation to the diverse hierarchies of interactions of microbes with one another and with the host biotic and abiotic environments. Many current definitions fail to capture this complexity and describe the term microbiome as encompassing the genomes of microorganisms only.

In 2020, a panel of international experts, organised by the EU-funded MicrobiomeSupport project, published the results of their deliberations on the definition of the microbiome. The panel was composed of about 40 leaders from diverse microbiome areas, and about one hundred further experts from around the world contributed through an online survey. They proposed a definition of the microbiome based on a revival of what they characterised as the "compact, clear, and comprehensive description of the term" as originally provided by Whipps ''et al''. in 1988, amended with a set of recommendations considering subsequent technological developments and research findings. They clearly separate the terms microbiome and microbiota and provide a comprehensive discussion considering the composition of microbiota, the heterogeneity and dynamics of microbiomes in time and space, the stability and resilience of microbial networks, the definition of core microbiomes, and functionally relevant keystone species as well as co-evolutionary principles of microbe-host and inter-species interactions within the microbiome.

The panel extended the Whipps ''et al''. definition, which contains all important points that are valid even 30 years after its publication in 1988, by two explanatory paragraphs differentiating the terms microbiome and microbiota and pronouncing its dynamic character, as follows:

* The ''microbiome'' is defined as a characteristic microbial community occupying a reasonable well-defined habitat which has distinct physio-chemical properties. The microbiome not only refers to the microorganisms involved but also encompass their theatre of activity, which results in the formation of specific ecological niches. The microbiome, which forms a dynamic and interactive micro-ecosystem prone to change in time and scale, is integrated in macro-ecosystems including eukaryotic hosts, and here crucial for their functioning and health.

* The ''microbiota'' consists of the assembly of microorganisms belonging to different kingdoms (prokaryotes (bacteria, archaea), eukaryotes (algae, protozoa, fungi etc), while "their theatre of activity" includes microbial structures, metabolites, mobile genetic elements (such as transposons, phages, and viruses), and relic DNA embedded in the environmental conditions of the habitat.

Membership

Microbiota

The microbiota comprises all living members forming the microbiome. Most microbiome researchers agree bacteria, archaea, fungi, algae, and small protists should be considered as members of the microbiome. The integration of phages, viruses, plasmids, and mobile genetic elements is a more controversial issue in the definition of the microbiome. There is also no clear consensus as to whether extracellular DNA derived from dead cells, so-called "relic DNA", belongs to the microbiome. Relic DNA can be up to 40% of the sequenced DNA in soil, and was up to 33% of the total bacterial DNA on average in a broader analysis of habitats with the highest proportion of 80% in some samples. Despite its omnipresence and abundance, relic DNA had a minimal effect on estimates of taxonomic and phylogenetic diversity.

When it comes to the use of specific terms, a clear differentiation between microbiome and microbiota helps to avoid the controversy concerning the members of a microbiome. Microbiota is usually defined as the assemblage of living microorganisms present in a defined environment. As phages, viruses, plasmids, prions, viroids, and free DNA are usually not considered as living microorganisms, they do not belong to the microbiota.

The term microbiome, as it was originally postulated by Whipps and coworkers, includes not only the community of the microorganisms but also their "theatre of activity". The latter involves the whole spectrum of molecules produced by the microorganisms, including their structural elements (nucleic acids, proteins, lipids, polysaccharides), metabolites (signalling molecules, toxins, organic, and inorganic molecules), and molecules produced by coexisting hosts and structured by the surrounding environmental conditions. Therefore, all mobile genetic elements, such as phages, viruses, and "relic" and extracellular DNA, should be included in the term microbiome, but are not a part of microbiota. The term microbiome is also sometimes confused with the metagenome. Metagenome is, however, clearly defined as a collection of genomes and genes from the members of a microbiota.

Microbiome studies sometimes focus on the behaviour of a specific group of microbiota, generally in relation to or justified by a clear hypothesis. More and more terms like bacteriome, archaeome, mycobiome, or virome have started appearing in the scientific literature, but these terms do not refer to biomes (a regional ecosystem with a distinct assemblage of (micro) organisms, and physical environment often reflecting a certain climate and soil) as the microbiome itself. Consequently, it would be better to use the original terms (bacterial, archaeal, or fungal community). In contrast to the microbiota, which can be studied separately, the microbiome is always composed by all members, which interact with each other, live in the same habitat, and form their ecological niche together. The well-established term ''virome'' is derived from virus and genome and is used to describe viral shotgun metagenomes consisting of a collection of nucleic acids associated with a particular ecosystem or holobiont. ''Viral metagenomes'' can be suggested as a semantically and scientifically better term.

Networks

File:Microbial interactions visualized through microbial co-occurrence networks.webp, Co-occurrence networks help visualising microbial interactions
Nodes usually represent taxa of microorganisms, and edges represent statistically significant associations between nodes.
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Testing of the hypotheses resulted from the network analyses is required for a comprehensive study of microbial interactions.

Microbes interact with one another, and these symbiotic interactions have diverse consequences for microbial fitness, population dynamics, and functional capacities within the microbiome. The microbial interactions can either be between microorganisms of the same species or between different species, genera, families, and domains of life. The interactions can be separated into positive, negative, and neutral types. Positive interactions include mutualism, synergism, and commensalism. Negative interactions include amensalism, predation, parasitism, antagonism, and competition. Neutral interactions are interactions where there is no observed effect on the functional capacities or fitness of interacting species microbial life strategy concepts.

File:Co-occurrence networks showing difference in gut microbiota between herbivorous and carnivorous cichlids.webp, Co-occurrence networks show difference in gut microbiota between herbivorous and carnivorous cichlids
Nodes coloured according to phylum. The herbivore network has higher complexity (156 nodes and 339 edges) compared to the carnivore network (21 nodes and 70 edges). Modified text was copied from this source, which is available under
Creative Commons Attribution 4.0 International License

Microbiomes exhibit different adaptive strategies. Oligotrophs are organisms that can live in an environment offering very low levels of nutrients, particularly carbon. They are characterised by slow growth, low rates of metabolism, and generally low population density. Oligotrophic environments include deep oceanic sediments, caves, glacial and polar ice, deep subsurface soil, aquifers, ocean waters, and leached soils. In contrast are the copiotrophs, which thrive in much higher carbon concentrations, and do well in high organic substrate conditions such as sewage lagoons.

In addition to oligotrophic and copiotrophic strategists, the competitor–stress tolerator–ruderals framework can influence the outcomes of interactions. For example, microorganisms competing for the same source can also benefit from each other when competing for the same compound at different trophic levels. Stability of a complex microbial ecosystem depends on trophic interactions for the same substrate at different concentration levels. As of 2020 microbial social adaptations in nature have been understudied. Here molecular markers can provide insight into social adaptations by supporting the theories, e.g., of altruists and cheaters in native microbiomes.

Coevolution

File:Shift of microbial-host coevolution from separation theories to a holistic approach.webp, In a holistic approach, the hosts and their associated microbiota are assumed to have coevolved with each other, alt=from "separation" theories to a holistic approach In a holistic approach, the hosts and their associated microbiota are assumed to have coevolved with each other

According to the "separation" approach, the microorganisms can be divided into pathogens, neutral, and symbionts, depending on their interaction with their host. The coevolution between host and its associated microbiota may be accordingly described as antagonistic (based on negative interactions) or mutualistic (based on positive interactions).

As of 2020, the emergence in publications about opportunistic pathogens and pathobionts has produced a shift towards a holistic approach in the coevolutions theory. The holistic approach sees the host and its associated microbiota as one unit (the so-called holobiont), that coevolves as one entity. According to the holistic approach, holobiont's disease state is linked to dysbiosis, low diversity of the associated microbiota, and their variability: a so-called pathobiome state. The healthy state, on the other hand, is accompanied with eubiosis, high diversity, and uniformity of the respective microbiota.

Types

Terrestrial

Plant

File:Microbiome in plant ecosystem.jpg, Microbiomes in the plant ecosystem, alt=Microbiomes in the plant ecosystem

The plant microbiome plays roles in plant health and food production and has received significant attention in recent years.. Modified text was copied from this source, which is available under
Creative Commons Attribution 4.0 International License
Plants live in association with diverse microbial consortia. These microbes, referred to as the plant's microbiota, live both inside (the endosphere) and outside (the episphere) of plant tissues, and play important roles in the ecology and physiology of plants. Modified text was copied from this source, which is available under
Creative Commons Attribution 4.0 International License
"The core plant microbiome is thought to comprise keystone microbial taxa that are important for plant fitness and established through evolutionary mechanisms of selection and enrichment of microbial taxa containing essential functions genes for the fitness of the plant holobiont".

Plant microbiomes are shaped by both factors related to the plant itself, such as genotype, organ, species and health status, as well as factors related to the plant's environment, such as management, land use and climate. The health status of a plant has been reported in some studies to be reflected by or linked to its microbiome.

Plant and plant-associated microbiota colonise different niches on and inside the plant tissue. All the above-ground plant parts together, called the phyllosphere, are a continuously evolving habitat due to ultraviolet (UV) radiation and altering climatic conditions. It is primarily composed of leaves. Below-ground plant parts, mainly roots, are generally influenced by soil properties. Harmful interactions affect the plant growth through pathogenic activities of some microbiota members. On the other hand, beneficial microbial interactions promote plant growth. Modified text was copied from this source, which is available under
Creative Commons Attribution 4.0 International License

The addition of synthetic nitrogen fertiliser may have little impact on soil microbiome structure or composition, but drastically reduces the microbiome network connectivity.

Animal

File:Principal-coordinate analysis of animal microbiome data sets.jpg, Principal coordinate analysis of animal gut microbiome data, alt=Principal coordinate analysis of animal gut microbiome data

The mammalian gut microbiome has emerged as a key regulator of host physiology, and coevolution between host and microbial lineages has played a key role in the adaptation of mammals to their diverse lifestyles. Diet, especially herbivory, is an important correlate of microbial diversity in mammals. Most mammalian microbiomes are also strongly correlated with host phylogeny, despite profound shifts in diet. This suggests host factors that themselves change across host phylogeny, such as gut physiology, play an important role in structuring the gut microbiomes across mammals. The vertebrate adaptive immune system is even speculated to have evolved as just such a factor for selective maintenance of symbiotic homeostasis. Modified text was copied from this source, which is available under
Creative Commons Attribution 4.0 International License

The importance of phylogeny-correlated factors to the diversity of vertebrate microbiomes more generally is still poorly understood. Phylosymbiosis, or the observation that more closely related host species have more similar microbiomes, has been described in a number of nonmammalian taxa. Other analyses have found substantial variation in phylosymbiotic signals among mammalian taxa, sometimes with conflicting results. The presence of a robust phylosymbiotic correlation implies that host factors control microbial assembly. Even if the specific mechanisms are unknown, variation in the strength or presence of a measurable phylosymbiotic signal across host phylogeny could prove useful for identifying such mechanisms through comparative studies. However, as of 2020 most studies have focused on just a few taxa at a time, and variable methods for both surveying the microbiome and measuring phylosymbiosis and host specificity (or the restriction of microbes to specific host lineages) have made generalisations difficult.

Without broader evolutionary context, it is unclear how universally conserved patterns of host-microbe phylosymbiosis actually are. Growing evidence indicates that the strong patterns identified in mammals are the exception rather than the rule in vertebrates. Meta-analyses of fish and birds have failed to detect the strength of correlations to diet and phylogeny reported in mammals. A recent analysis of samples from more than 100 vertebrate species also found the strength of phylogenetic correlation to be much higher in mammals than in birds, reptiles, amphibians, or fish. It is increasingly appreciated in nonvertebrate animals that fundamental aspects of the host's relationship to its symbiotic community can change drastically between taxa: many insects depend entirely on microbes for key metabolites, while others seem to be devoid of resident gut microbes.

Human

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-animal

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