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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. [1]
The idea of holism started to regain popularity in biology when the endosymbiosis theory was first proposed by Konstantin Mereschkowski in 1905 and further developed by Ivan Wallin in 1925. Still accepted today, this theory posits a single origin for eukaryotic cells through the symbiotic assimilation of prokaryotes to form first mitochondria and later plastids (the latter through several independent symbiotic events) via phagocytosis (reviewed in Archibald, 2015). [2] These ancestral and founding symbiotic events, which prompted the metabolic and cellular complexity of eukaryotic life, most likely occurred in the ocean. [3] [1]
Despite the general acceptance of the endosymbiosis theory, the term holobiosis or holobiont did not immediately enter the scientific vernacular. It was coined independently by the German Adolf Meyer-Abich in 1943, [4] [5] and by Lynn Margulis in 1990, who proposed that evolution has worked mainly through symbiosis-driven leaps that merged organisms into new forms, referred to as “holobionts”, and only secondarily through gradual mutational changes. [6] [7] However, the concept was not widely used until it was co-opted by coral biologists over a decade later. Corals and the dinoflagellate algae called Zooxanthellae are one of the most iconic examples of symbioses found in nature; most corals are incapable of long-term survival without the products of photosynthesis provided by their endosymbiotic algae. Rohwer et al. (2002) [8] were the first to use the word holobiont to describe a unit of selection sensu Margulis [9] for corals, where the holobiont comprised the cnidarian polyp (host), Zooxanthellae algae, various ectosymbionts (endolithic algae, prokaryotes, fungi, other unicellular eukaryotes), and viruses. [1]
Although initially driven by studies of marine organisms, much of the research on the emerging properties and significance of holobionts has since been carried out in other fields of research: the microbiota of the rhizosphere of plants or the animal gut became predominant models and have led to an ongoing paradigm shift in agronomy and medical sciences. [10] [11] [12] Holobionts occur in terrestrial and aquatic habitats alike, and several analogies between these ecosystems can be made. For example, in all of these habitats, interactions within and across holobionts such as induction of chemical defenses, nutrient acquisition, or biofilm formation are mediated by chemical cues and signals in the environment, dubbed infochemicals. [13] [14] [15] [16] Nevertheless, we can identify two major differences between terrestrial and aquatic systems. First, the physicochemical properties of water result in higher chemical connectivity and signaling between macro- and micro-organisms in aquatic or moist environments. In marine ecosystems, carbon fluxes also appear to be swifter and trophic modes more flexible, leading to higher plasticity of functional interactions across holobionts. [17] Moreover, dispersal barriers are usually lower, allowing for faster microbial community shifts in marine holobionts. [18] [19] Secondly, phylogenetic diversity at broad taxonomic scales (i.e., supra-kingdom, kingdom and phylum levels), is higher in aquatic realms compared to land, with much of the aquatic diversity yet to be uncovered, [20] [21] especially marine viruses. [22] [23] [24] [1]
The boundaries of holobionts are usually delimited by a physical gradient, which corresponds to the area of local influence of the host, e.g., in unicellular algae the so-called phycosphere. [25] However, they may also be defined in a context-dependent way as a Russian matryoshka doll, setting the boundaries of the holobiont depending on the interactions and biological functions that are being considered. Thus holobionts may encompass all levels of host-symbiont associations from intimate endosymbiosis with a high degree of co-evolution up to the community and ecosystem level; a concept referred to as "nested ecosystems" (see diagram). [26] [27] [1]
In the diagram on the right, the host (blue circles), and associated microbes (all other shapes) including bacteria and eukaryotes that may be inside (i.e., endosymbiotic) or outside the host (i.e., ectosymbiotic) are connected by either beneficial (solid orange lines), neutral (solid blue lines) or pathogenic (dashed black lines) interactions, respectively. Changes from beneficial or neutral to pathogenic interactions are typical cases of dysbiosis. The different clusters are illustrated by the following examples: 1, a model holobiont in a stable physiological condition (e.g., in controlled laboratory condition); 2 and 3, holobionts changing during their life cycle or subjected to stress conditions—examples of vertically transmitted microbes are indicated by light blue arrows; 4 and 5, marine holobionts in the context of global sampling campaigns or long-term time series—examples of horizontal transmission of microbes and holobionts are illustrated by pink arrows. [1]
Such a conceptual perspective raises fundamental questions not only regarding the interaction between the different components of holobionts and processes governing their dynamics, but also of the relevant units of selection and the role of coevolution. For instance, plant and animal evolution involves new functions co-constructed by members of the holobiont or elimination of functions redundant among them, [28] and it is likely that these processes are also relevant in marine holobionts. Eugene Rosenberg et al. have argued that all animals and plants can be considered holobionts, and thus advocate the hologenome theory of evolution, suggesting that natural selection acts at the level of the holobiont and its hologenome. [29] [30] This interpretation of Margulis' definition of a holobiont considerably broadened fundamental concepts in evolution and speciation and has not been free of criticism, [31] especially when applied at the community or ecosystem level. [32] More recently, it has been shown that species that interact indirectly with the host can also be important in shaping coevolution within mutualistic multi-partner assemblages. [33] Thus, the holobiont concept and the underlying complexity of holobiont systems should be better defined and further considered when addressing evolutionary and ecological questions. [1]
Work on model systems has demonstrated that motile and macroscopic marine holobionts can act as dissemination vectors for geographically restricted microbial taxa. Pelagic mollusks or vertebrates are textbook examples of high dispersal capacity organisms (e.g., against currents and through stratified water layers). It has been estimated that fish and marine mammals may enhance the original dispersion rate of their microbiota by a factor of 200 to 200,000 [57] and marine birds may even act as bio-vectors across ecosystem boundaries. [58] This host-driven dispersal of microbes can include non-native or invasive species as well as pathogens. [57] [1]
A related ecological function of holobionts is their potential to sustain rare species. Hosts provide an environment that favors the growth of specific microbial communities distinct from the surrounding environment (including rare microbes). They may, for instance, provide a nutrient-rich niche in the otherwise nutrient-poor surroundings. [59] [60] [61] [62] [63] [1]
Lastly, biological processes regulated by microbes are important drivers of global biogeochemical cycles. [64] [65] [66] In the open ocean, it is estimated that symbioses with the cyanobacterium UCYN-A contribute about 20% to total N2 fixation. [67] [68] In benthic systems, sponges and corals may support entire ecosystems via their involvement in nutrient cycling thanks to their microbial partners, [69] [70] [71] [27] functioning as sinks and sources of nutrients. In particular the “sponge loop” recycles dissolved organic matter and makes it available to higher trophic levels in the form of detritus. [72] [70] [73] In coastal sediments, bivalves hosting methanogenic archaea have been shown to increase the benthic methane efflux by a factor of up to eight, potentially accounting for 9.5% of total methane emissions from the Baltic Sea. [74] This metabolic versatility is accomplished because of the simultaneous occurrence of disparate biochemical machineries (e.g., aerobic and anaerobic pathways) in individual symbionts, providing new metabolic abilities to the holobiont, such as the synthesis of specific essential amino acids, photosynthesis, or chemosynthesis. [34] [75] Furthermore, the interaction between host and microbiota can potentially extend the metabolic capabilities of a holobiont in a way that augments its resilience to environmental changes, [76] [77] [78] [79] [80] or allow it to cross biotope boundaries (e.g., Woyke et al., 2006) and colonize extreme environments (Bang et al., 2018). Holobionts thus contribute to marine microbial diversity and possibly resilience in the context of global environmental changes [57] and it is paramount to include the holobiont concept in predictive models that investigate the consequences of human impacts on the marine realm and its biogeochemical cycles. [1]
Two critical challenges partially addressed by using model systems are (1) to decipher the factors determining holobiont composition and (2) to elucidate the impacts and roles of the different partners in these complex systems over time. Some marine organisms such as bivalves transmit part of the microbiota maternally. [81] [82] In other marine holobionts, vertical transmission may be weak and inconsistent, whereas mixed modes of transmission (vertical and horizontal) or intermediate modes (pseudo-vertical, where horizontal acquisition frequently involves symbionts of parental origin) are more common. [83] Identifying the factors shaping holobiont composition and understanding their evolution is highly relevant for marine organisms given that most marine hosts display a high specificity for their microbiota and even patterns of phylosymbiosis, [84] [85] [86] despite a highly connected and microbe-rich environment. [1]
During microbiota transmission (whether vertical or horizontal), selection by the host and/or by other components of the microbiome, is a key process in establishing or maintaining a holobiont microbial community that is distinct from the environment. The immune system of the host, e.g., via the secretion of specific antimicrobial peptides, [87] [88] is one way of performing this selection in both marine and terrestrial holobionts. [1]
Another way of selecting a holobiont microbial community is by chemically mediated microbial gardening. This concept has been demonstrated for land plants, where root exudates manipulate microbiome composition. [89] In marine environments, the phylogenetic diversity of hosts and symbionts suggests both conserved and marine-specific chemical interactions, but studies are still in their infancy. For instance, seaweeds can chemically garden beneficial microbes, facilitating normal morphogenesis and increasing disease resistance, [52] [90] and seaweeds and corals structure their surface-associated microbiome by producing chemoattractants and antibacterial compounds. [14] [91] There are fewer examples of chemical gardening in unicellular hosts, but it seems highly likely that similar processes are in place. [92] [93] [1]
In addition to selection, ecological drift, dispersal and evolutionary diversification have been proposed as key processes in community assembly, but are difficult to estimate in microbial communities. [94] The only data currently at our disposal to quantify these processes are the diversity and distribution of microbes. Considering the high connectivity of aquatic environments, differences in marine microbial communities are frequently attributed to a combination of selection and drift, rather than limited dispersal, [61] a conclusion which in the future could be refined by conceptual models developed for instance for soil microbial communities. [93] [95] ) Diversification is mainly considered in the sense of coevolution or adaptation to host selection, which may also be driven by the horizontal acquisition of genes. However, cospeciation is challenging to prove [96] [32] and only few studies have examined this process in marine holobionts to date, each focused on a restricted number of actors. [97] [98] [1]
Perturbations in the transmission or the recruitment of the microbiota can lead to dysbiosis, and eventually microbial infections. [28] [93] Dysbiotic microbial communities are frequently determined by stochastic processes and thus display higher variability in their composition than those of healthy individuals. This observation in line with the "Anna Karenina principle", [99] although there are exceptions to this rule. [93] A specific case of dysbiosis is the so-called "Rasputin effect" where benign endosymbionts opportunistically become detrimental to the host due to processes such as reduction in immune response under food deprivation, coinfections, or environmental pressure. [100] Many diseases are now interpreted as the result of a microbial imbalance and the rise of opportunistic or polymicrobial infections upon host stress. [101] For instance in reef-building corals, warming destabilizes cnidarian-dinoflagellate associations, and some beneficial Symbiodiniacea strains switch their physiology and sequester more resources for their own growth at the expense of the coral host, leading to coral bleaching and even death. [102] [1]
Increasing our knowledge on the contribution of these processes to holobiont community assembly in marine systems is a key challenge, which is of particular urgency today in the context of ongoing global change. Moreover, understanding how the community and functional structure of resident microbes are resilient to perturbations remains critical to predict and promote the health of their host and the ecosystem. Yet, the contribution of the microbiome is still missing in most quantitative models predicting the distribution of marine macro-organisms, or additional information on biological interactions would be required to make the former more accurate. [103] [1]
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.
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.
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.
Marine microorganisms are defined by their habitat as microorganisms living in a marine environment, that is, in the saltwater of a sea or ocean or the brackish water of a coastal estuary. A microorganism is any microscopic living organism or virus, that is too small to see with the unaided human eye without magnification. Microorganisms are very diverse. They can be single-celled or multicellular and include bacteria, archaea, viruses and most protozoa, as well as some fungi, algae, and animals, such as rotifers and copepods. Many macroscopic animals and plants have microscopic juvenile stages. Some microbiologists also classify viruses as microorganisms, but others consider these as non-living.
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.
The root microbiome is the dynamic community of microorganisms associated with plant roots. Because they are rich in a variety of carbon compounds, plant roots provide unique environments for a diverse assemblage of soil microorganisms, including bacteria, fungi, and archaea. The microbial communities inside the root and in the rhizosphere are distinct from each other, and from the microbial communities of bulk soil, although there is some overlap in species composition.
The phycosphere is a microscale mucus region that is rich in organic matter surrounding a phytoplankton cell. This area is high in nutrients due to extracellular waste from the phytoplankton cell and it has been suggested that bacteria inhabit this area to feed on these nutrients. This high nutrient environment creates a microbiome and a diverse food web for microbes such as bacteria and protists. It has also been suggested that the bacterial assemblages within the phycosphere are species-specific and can vary depending on different environmental factors.
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.
The initial acquisition of microbiota is the formation of an organism's microbiota immediately before and after birth. The microbiota are all the microorganisms including bacteria, archaea and fungi that colonize the organism. The microbiome is another term for microbiota or can refer to the collected genomes.
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.
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.
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.
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. While the term hologenome originated from the hologenome theory of evolution, which postulates that natural selection occurs on the holobiont level, hologenomics uses an integrative framework to investigate interactions between the host and its associated species. Examples include gut microbe or viral genomes linked to human or animal genomes for host-microbe interaction research. Hologenomics approaches have also been used to explain genetic diversity in the microbial communities of marine sponges.
Endozoicomonas gorgoniicola is a Gram-negative and facultative anaerobic bacterium from the genus of Endozoicomonas. Individual cells are motile and rod-shaped. Bacteria in this genus are symbionts of coral. E. gorgoniicola live specifically with soft coral and were originally isolated from a species of Plexaura, an octocoral, off the coast of Bimini in the Bahamas. The presence of this bacterium in a coral microbiome is associated with coral health.
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.
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 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".
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.