Microbiome

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.[2][3] It was defined 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".[4]

The term microbiome encompasses both the microbiota (community of microorganisms) and their "theatre of activity" (structural elements, metabolites/signal molecules, and the surrounding environmental conditions.[1]

In 2020, an international panel of experts published the outcome of their discussions on the definition of the microbiome.[1] 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 sentences.[1]

The first explanatory sentence pronounces the dynamic character of the microbiome:

  • The microbiome is defined as a characteristic microbial community occupying a reasonably 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.[1]

The second explanatory sentence clearly separates the term microbiota from the term microbiome:

  • The microbiota consists of the assembly of microorganisms belonging to different kingdoms (Prokaryotes [Bacteria, Archaea], Eukaryotes [e.g., Protozoa, Fungi, and Algae]), 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.[1]

Background
Timeline of microbiome research from seventeenth century [1]

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.[1]

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.[1]

Paradigm shift
Highlighting the shift of the paradigm from microbes as unsocial organisms causing diseases to the holistic view of microorganisms being the center of the One Health Concept: positively interconnecting all areas of human lives.[1]

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. 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.[5][6][1]

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.[7] 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.[8][1]

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.[9] Today, we are able to 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.[10][11][12][1]

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.[13] 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.[14][15] 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.[16][17][1]

Defining the microbiome

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.[18] In 1988, Whipps and colleagues working on the ecology of rhizosphere microorganisms provided the first definition of the term microbiome.[4] 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.[1]

However, many other microbiome definitions have been published in the last few decades. The currently most cited definition by Lederberg[19] describes 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.[20] 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[21] 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 (see table ↓).[1]

Microbiome definitions[1]
Definition type Examples
Ecological Definitions based on ecology describe the microbiome following the concepts derived from the ecology of multicellular organisms. The main issue here is that the theories from the macro-ecology do not always fit the rules in the microbial world.
  • "A convenient ecological framework in which to examine biocontrol systems is that of the microbiome. This may be 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".[4]
  • "This term refers to the entire habitat, including the microorganisms (bacteria, archaea, lower and higher eurkaryotes, and viruses), their genomes (i.e., genes), and the surrounding environmental conditions. This definition is based on that of “biome,” the biotic and abiotic factors of given environments. Others in the field limit the definition of microbiome to the collection of genes and genomes of members of a microbiota. It is argued that this is the definition of metagenome, which combined with the environment constitutes the microbiome. The microbiome is characterized by the application of one or combinations of metagenomics, metabonomics, metatranscriptomics, and metaproteomics combined with clinical or environmental metadata".[20]
  • "others use the term microbiome to mean all the microbes of a community, and in particular, for the plant microbiome, those microbial communities associated with the plant which can live, thrive, and interact with different tissues such as roots, shoots, leaves, flowers, and seeds".[22]
  •  "Ecological community of commensal, symbiotic and pathogenic microorganisms within a body space or other environment".[19]
Organisms/host-dependent The host-dependent definitions are based on the microbial interactions with the host. The main gaps here concern the question whether the microbial-host interaction data gained from one host can be transferred to another. The understanding of coevolution and selection in the host-dependent definitions is also underrepresented.
  • "A community of microorganisms (such as bacteria, fungi, and viruses) that inhabit a particular environment and especially the collection of microorganisms living in or on the human body".[23]
  • "Human Microbiome Project (HMP): [...] The Human Microbiome is the collection of all the microorganisms living in association with the human body. These communities consist of a variety of microorganisms including eukaryotes, archaea, bacteria and viruses".[24]
Genomic/ method-driven There is a variety of microbiome definitions available that are driven by the methods applied. Mostly, these definitions rely on DNA sequence-based analysis and describe microbiome as a collective genome of microorganisms in a specific environment. The main bottleneck here is that every new available technology will result in a need for a new definition.
  •  "The collective genomes of microorganisms inhabiting a particular environment and especially the human body".[23]
  •  "The microbiome comprises all of the genetic material within a microbiota (the entire collection of microorganisms in a specific niche, such as the human gut). This can also be referred to as the metagenome of the microbiota".[25]
  •  "Microbiome is a term that describes the genome of all the microorganisms, symbiotic and pathogenic, living in and on all vertebrates. The gut microbiome consists of the collective genome of microbes inhabiting the gut including bacteria, archaea, viruses, and fungi".[26]
  •  "Different approaches to define the population provide different information. a | Microbiota: 16S rRNA surveys are used to taxonomically identify the microorganisms in the environment. b | Metagenome: the genes and genomes of the microbiota, including plasmids, highlighting the genetic potential of the population. c | Microbiome: the genes and genomes of the microbiota, as well as the products of the microbiota and the host environment".[27]
  •  "Totality of genomes of a microbiota. Often used to describe the entity of microbial traits (=functions) encoded by a microbiota."[28]
Combined There are some microbiome definitions available that fit several categories with their advantages and disadvantages.
  •  "A microbiome is the ecological community of commensal, symbiotic, and pathogenic microorganisms that literally share our body space."[29]
  •  "The microbiome is the sum of the microbes and their genomic elements in a particular environment".[30]
  •  "The genes and genomes of the microbiota, as well as the products of the microbiota and the host environment".[31]

In 2020, a panel of international experts, organised by the EU-funded MicrobiomeSupport project,[32] published the results of their deliberations on the definition of the microbiome.[1] 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 the compact, clear, and comprehensive description of the term as originally provided by Whipps et al. in 1988,[4] 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.[1]

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 sentences 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.[1]
  • 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.[1]

Microbiota – members of the microbiome
Main article: 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.[20][1] 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.[33][1] Relic DNA can be up to 40% of the sequenced DNA in soil,[34] 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.[35] Despite its omnipresence and abundance, relic DNA had a minimal effect on estimates of taxonomic and phylogenetic diversity.[35][1]

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.[1] Microbiota is usually defined as the assemblage of living microorganisms present in a defined environment.[20] As phages, viruses, plasmids, prions, viroids, and free DNA are usually not considered as living microorganisms,[36] they do not belong to the microbiota.[1]

The term microbiome, as it was originally postulated by Whipps and coworkers,[4] 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.[20][1]

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.[1] 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.[37] Viral metagenomes can be suggested as a semantically and scientifically better term.[1]

Plant microbiomes
Representative microbial networks in different plant habitats [38]
Main article: Plant microbiome

The diagram on the right →
illustrates microbial communities in the soil, air, rhizosphere, phyllosphere, and inside plant tissue (endosphere). In each of these habitats, microbes (represented by colored circles) could interact positively, negatively, or do not interact with other microbes (no lines). Specific microbes, often defined as “hub” or “keystone” species (circles highlighted in bold), are highly connected to other microbes within the networks and likely exert a stronger influence on the structure of microbial communities. (a) Root-associated microbes mainly derive from the soil biome. (b) Leaf-associated microbes originate from various sources such as aerosols, insects, or dust. (c) Relocation between aboveground and belowground microbiota members.[38]

The microbial component of healthy seeds – the seed microbiome – appears to be inherited between plant generations and can dynamically influence germination, plant performance, and survival.[39] As such, methods to optimize the seed microbiomes of major crops could have far-reaching implications for plant breeding and crop improvement to enhance agricultural food, feed, and fiber production.[40]

Introducing beneficial bacteria into plant seed
(A) Plant flowers are sprayed with a bacterial suspension. (B) The bacteria colonize flowers and the developing seeds. (C) Mature seeds are collected and endophytes stay viable during seed storage. (D) Endophytes proliferate during germination and colonize the offspring plant generation.[40]

Marine microbiomes
Marine animal host-microbiome relationship
Relationships are generally thought to exist in a symbiotic state, and are normally exposed to environmental and animal-specific factors that may cause natural variations. Some events may change the relationship into a functioning but altered symbiotic state, whereas extreme stress events may cause dysbiosis or a breakdown of the relationship and interactions.[41]

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 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.[41]

The microbiomes of diverse marine animals are currently under study, from simplistic organisms including sponges[42] and ctenophores [43] to more complex organisms such as sea squirts[44] and sharks.[45][41]

The relationship between the Hawaiian bobtail squid and the bioluminescent bacterium Aliivibrio fischeri is one of the best studied symbiotic relationships in the sea and is a choice system for general symbiosis research. This relationship has provided insight into fundamental processes in animal-microbial symbioses, and especially biochemical interactions and signaling between the host and bacterium.[46][47][41]

The gutless marine oligochaete worm Olavius algarvensis is another relatively well-studied marine host to microbes. These three centimetre long worms reside within shallow marine sediments of the Mediterranean Sea. The worms do not contain a mouth or a digestive or excretory system, but are instead nourished with the help of a suite of extracellular bacterial endosymbionts that reside upon coordinated use of sulfur present in the environment.[48] This system has benefited from some of the most sophisticated 'omics and visualization tools.[49] For example, multi-labeled probing has improved visualization of the microbiome[50] and transcriptomics and proteomics have been applied to examine host–microbiome interactions, including energy transfer between the host and microbes[51] and recognition of the consortia by the worm's innate immune system.[52] The major strength of this system is that it does offer the ability to study host–microbiome interactions with a low diversity microbial consortium, and it also offers a number of host and microbial genomic resources[49][53][41]

Stylophora pistillata coral colony and the bacteria Endozoicomonas (Ez) probed cells (yellow) within the tentacles of S. pistillata residing in aggregates (Ez agg) as well as just outside the aggregate (b).[54]

Corals are one of the more common examples of an animal host whose symbiosis with microalgae can turn to dysbiosis, and is visibly detected as bleaching. Coral microbiomes have been examined in a variety of studies, which demonstrate how variations in the ocean environment, most notably temperature, light, and inorganic nutrients, affect the abundance and performance of the microalgal symbionts, as well as calcification and physiology of the host.[55][56] Studies have also suggested that resident bacteria, archaea, and fungi additionally contribute to nutrient and organic matter cycling within the coral, with viruses also possibly playing a role in structuring the composition of these members, thus providing one of the first glimpses at a multi-domain marine animal symbiosis.[57] The gammaproteobacterium Endozoicomonas is emerging as a central member of the coral's microbiome, with flexibility in its lifestyle.[54][58] Given the recent mass bleaching occurring on reefs,[59] corals will likely continue to be a useful and popular system for symbiosis and dysbiosis research.[41]

Sponges are common members of the ocean's diverse benthic habitats and their abundance and ability to filter large volumes of seawater have led to the awareness that these organisms play critical roles in influencing benthic and pelagic processes in the ocean.[60] They are one of the oldest lineages of animals, and have a relatively simple body plan that commonly associates with bacteria, archaea, algal protists, fungi, and viruses.[61] Sponge microbiomes are composed of specialists and generalists, and complexity of their microbiome appears to be shaped by host phylogeny.[62] Studies have shown that the sponge microbiome contributes to nitrogen cycling in the oceans, especially through the oxidation of ammonia by archaea and bacteria.[63][64] Most recently, microbial symbionts of tropical sponges were shown to produce and store polyphosphate granules,[65] perhaps enabling the host to survive periods of phosphate depletion in oligotrophic marine environments.[66] The microbiomes of some sponge species do appear to change in community structure in response to changing environmental conditions, including temperature[67] and ocean acidification,[68][69] as well as synergistic impacts.[70]

Underlying complexity
Tradeoffs between experimental questions and complexity of microbiome systems [71]

Each microbiome system is suited to address different types of questions based on the culturability of microbes, genetic tractability of microbes and host (where relevant), ability to maintain system in laboratory setting, and ability to make host/environment germfree.[71]

Three different systems are shown in the figure on the right. (A) Pairwise interactions between the soil bacteria Bacillus subtilis and Streptomyces spp. are well-suited for characterizing the functions of secondary metabolites in microbial interactions. (B) The symbiosis between bobtail squid and the marine bacterium Aliivibrio fischeri is fundamental to understanding host and microbial factors that influence colonization. (C) The use of gnotobiotic mice is crucial for making links between host diet and the effects on specific microbial taxa in a community.[71]

Host-microbe coevolution
Shift in the understanding of the microbial-host coevolution 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.[1]
See also: Holobiont and Hologenome theory of evolution

According to the "separation" approach (upper part of the figure on the right), 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).[1]

As of 2020, the emergence in publications about opportunistic pathogens and pathobionts has produced a shift towards a holistic approach in the coevolutions theory (lower part of the figure on the right). 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.[1]

See also

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