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Now characterised by high-throughput sequencing methods that enable the study of microbes without lab culture, the human "microbiome" (the microbial flora of the body) is said to have revolutionary implications for biology and medicine. According to many experts, we must now understand ourselves as "holobionts" like lichen or coral, multispecies superorganisms that consist of animal and symbiotic microbes in combination, because normal physiological function depends on them. Here I explore the 1960s research of biologist René Dubos, a forerunner figure mentioned in some historical accounts of the microbiome, and argue that he arrived at the superorganism concept 40 years before the Human Microbiome Project. This raises the question of why his contribution was not hailed as revolutionary at the time and why Dubos is not remembered for it. [ABSTRACT FROM AUTHOR]

Definition: Lichens have long been considered as composite organisms composed of algae and/or cyanobacteria hosted by a fungus in a mutualistic relationship. Other organisms have been gradually discovered within the lichen thalli, such as multiple algal species, yeasts, or even viruses. Of pivotal relevance is the existence of the lichen microbiome, which is a community of microorganisms that can be found living together on the lichen surface. This community performs a growing number of functions. In this entry, we explore the journey of lichens being considered from a dual partnership to a multi-species symbiotic relationship. [ABSTRACT FROM AUTHOR]

The emergent concept of the social microbiome implies a view of a highly connected biological world, in which microbial interchange across organisms may be influenced by social and ecological connections occurring at different levels of biological organization. We explore this idea reviewing evidence of whether increasing social complexity in primate societies is associated with both higher diversity and greater similarity in the composition of the gut microbiota. By proposing a series of predictions regarding such relationship, we evaluate the existence of a link between gut microbiota and primate social behavior. Overall, we find that enough empirical evidence already supports these predictions. Nonetheless, we conclude that studies with the necessary, sufficient, explicit, and available evidence are still scarce. Therefore, we reflect on the benefit of founding future analyses on the utility of social complexity as a theoretical framework. [ABSTRACT FROM AUTHOR]

Holobionts formed by a host organism and associated symbionts are key biological units in marine ecosystems where they are responsible for fundamental ecosystem services. Therefore, understanding anthropogenic impacts on holobionts is essential. Sponges (Phylum Porifera) are ideal holobiont models. They host a complex microbial community and provide ecosystem services including nutrient cycling. At bathyal depths, sponges can accumulate forming dense sponge ground habitats supporting biodiverse associated communities. However, the impacts of spilled oil and dispersants on sponge grounds cannot be understood without considering exposures mediated through sponge filtration of marine snow particles. To examine this, we exposed the model sponge Halichondria panicea to oil, dispersant and "marine oil snow" contaminated seawater and elucidate the complex molecular response of the holobiont through metatranscriptomics. While the host response included detoxification and immune response pathways, the bacterial symbiotic response differed and was at least partially the result of a change in the host environment rather than a direct response to hydrocarbon exposure. As the sponge host reduced its pumping activity and internal tissue oxygen levels declined, the symbionts changed their metabolism from aerobic to anaerobic pathways possibly via quorum sensing. Furthermore, we found evidence of hydrocarbon degradation by sponge symbionts, but sponge mortality (even when exposed to low concentrations of hydrocarbons) implied this may not provide the holobiont with sufficient resilience against contaminants. Given the continued proposed expansion of hydrocarbon production into deep continental shelf and slope settings where sponge grounds form significant habitats it is important that dispersant use is minimised and that environmental impact assessments carefully consider the vulnerability of sponge holobionts. [ABSTRACT FROM AUTHOR]

What can developmental biology contribute toward mitigating the consequences of anthropogenic assaults on the environment and climate change? In this Spotlight article, we advocate a developmental biology that takes seriously Lynn Margulis' claim that 'the environment is part of the body'. We believe this to be a precondition for developmental biology playing important roles in conservation and environmental restoration. We need to forge a developmental biology of the holobiont - the multi-genomic physiologically integrated organism that is also a functional biome. To this end, we highlight how developmental biology needs to explore more deeply the interactions between developing organisms, and their chemical, physical and biotic environments. [ABSTRACT FROM AUTHOR]

Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here, we integrate embryology and microbiology to review how symbiotic microorganisms are transmitted in this early-diverging lineage. We describe that vertical transmission is widespread but not universal, that microbes are vertically transmitted during a select developmental window, and that properties of the developmental microbiome depends on whether a species is a high or low microbial abundance sponge. Reproduction, development, and symbiosis are thus deeply rooted, but why these partnerships form remains the central and elusive tenet of these developmental symbioses. [ABSTRACT FROM AUTHOR]

Lynn Margulis has made it clear that in nature partnerships are the predominant form of life; that life processes can only be understood in terms of the interactions of such partnerships; and that their inherent complexity can only be understood by taking a holistic approach. Here I attempt to relate Lynn Margulis´ observations on the freshwater polyp hydra to the perceptions and problems of today's Hydra research. To accomplish this, I will synthesize our current understanding of how symbionts influence the phenotype and fitness of hydra. Based on this new findings, a fundamental paradigm shift and a new era is emerging in the way that we consider organisms such as hydra as multi-organismic metaorganisms, just as Lynn Margulis may have thought about it. [ABSTRACT FROM AUTHOR]

The importance of plants as complex entities influenced by genomes of the associated microorganisms is now seen as a new source of variability for a more sustainable agriculture, also in the light of ongoing climate change. For this reason, we investigated through metatranscriptomics whether the taxa profile and behaviour of microbial communities associated with the wood of 20-year-old grapevine plants are influenced by the health status of the host. We report for the first time a metatranscriptome from a complex tissue in a real environment, highlighting that this approach is able to define the microbial community better than referenced transcriptomic approaches. In parallel, the use of total RNA enabled the identification of bacterial taxa in healthy samples that, once isolated from the original wood tissue, displayed potential biocontrol activities against a wood-degrading fungal taxon. Furthermore, we revealed an unprecedented high number of new viral entities (~120 new viral species among 180 identified) associated with a single and limited environment and with potential impact on the whole holobiont. Taken together, our results suggest a complex multitrophic interaction in which the viral community also plays a crucial role in raising new ecological questions for the exploitation of microbial-assisted sustainable agriculture. [ABSTRACT FROM AUTHOR]

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Fleece rot develops following prolonged wetting of sheep when bacterial proliferation in wool and on skin induces exudation of serum proteins onto the skin surface and causes damage to wool follicles and fibres. These processes create an attractive environment for blowflies to lay eggs, leading to body strike. Current reliance on insecticides for prevention and treatment of fly strike is being increasingly challenged by development of insecticide resistance. This review examines the large body of past research on the bacterial causes of fleece rot, the genetics of sheep susceptibility and resistance, the characteristics of the resulting immune defence reactions, and attempts to control fleece rot by vaccination. The high dependence on weather conditions for expression of fleece rot hampers studies on the disease. Normal skin and wool are populated by a dynamic microbial community. During adverse environmental conditions, natural resistance to fleece rot associated with physical characteristics of wool and skin can be overwhelmed and a complex mix of bacteria flourishes. Prolonged hydration alone, and in combination with bacterial exoproducts, induces dermatitis and exudation of immunoglobulins and other serum proteins onto the skin surface. Pathogens do not usually penetrate the epidermis. Nonetheless, during prolonged skin hydration, sheep can become sensitised to fleece rot pathogens and produce antibodies. Antibody titres rise late within a typical (3 week) case of fleece rot. High naturally acquired antibody titres may contribute to resistance to fleece rot. In contrast to some evidence for a protective role of antibody, there is little evidence for innate or adaptive cellular immune responses contributing to protection against fleece rot pathogens. Previous attempts to develop vaccines have met with mixed success. Nonetheless, there remain prospects for development of a new vaccine to control fleece rot. Further knowledge on the microbial ecology of normal and wet skin would assist this endeavour and may help identify other control strategies. Following wetting for several days or more, bacteria proliferate on the skin and in the wool to cause fleece rot which predisposes sheep to fly strike. This review examines the bacteria associated with fleece rot, their role in the disease, sheep factors influencing susceptibility to infection, defences of the sheep against infection and past efforts to develop vaccines. This background sets the scene for an accompanying review on new opportunities for vaccine development. [ABSTRACT FROM AUTHOR]

Seaweeds account for nearly 30% of global aquaculture production by volume, and their cultivation provides important opportunities for employment and wealth generation, particularly in rural coastal communities. Eucheumatoids (Kappaphycus and Eucheuma spp.) are tropical red algae commercially cultivated as raw material for production of carrageenans, particularly in South‐East Asia and the Western Indian Ocean region. Diseases and pests are major limiting factors in eucheumatoid production, particularly a condition known as 'ice‐ice' disease (IID). IID is characterized by bleaching of the thallus followed by the disintegration of affected tissues, leading to a loss of biomass and reduced carrageenan yield. IID has been associated with unfavourable changes in environmental conditions, particularly an increase in sea water temperature and a decrease in salinity, and infection by opportunistic or pathogenic bacteria. However, given that no single or combined causal agents have been definitely identified, IID may be considered a complex pathobiotic syndrome in which multiple factors contribute to the development of disease signs. Here, we review current knowledge of the abiotic and biotic factors associated with the development of IID, and the strategies employed to mitigate economic losses resulting from disease outbreaks. We discuss syndromic diseases in other marine holobionts, particularly other red algae and corals, in relation to their similarity to IID, and suggest the application of comprehensive and complementary methodologies, including high‐throughput sequencing and high‐quality microscopy, for enhancing our understanding of the pathological and microbiological processes associated with IID signs. [ABSTRACT FROM AUTHOR]

Macroalgal holobiont studies involve understanding interactions between the host, its microbiota, and the environment. We analyzed the effect of bacteria–kelp interactions on phenotypic responses of two genetically distinct populations of giant kelp, Macrocystis pyrifera (north and south), exposed to different nitrogen (N) concentrations. In co‐culture experiments with different N concentration treatments, we evaluated kelp growth responses and changes in three specific molecular markers associated with the N cycle, both in epiphytic bacteria (relative abundance of nrfA‐gene: cytochrome c nitrite reductase) and macroalgae (expression of NR‐gene: nitrate reductase; GluSyn‐gene: glutamate synthase). Both kelp populations responded differently to N limitation, with M. pyrifera‐south sporophytes having a lower specific growth rate (SGR) under N‐limiting conditions than the northern population; M. pyrifera‐north sporophytes showed no significant differences in SGR when exposed to low‐N and high‐N concentrations. This corresponded to a higher GluSyn‐gene expression in the M. pyrifera‐north sporophytes and the co‐occurrence of specific nrfA bacterial taxa. These bacteria may increase ammonium availability under low‐N concentrations, allowing M. pyrifera‐north to optimize nutrient assimilation by increasing the expression of GluSyn. We conclude that bacteria–kelp interactions are important in enhancing kelp growth rates under low N availability, although this effect may be regulated by the genetic background of kelp populations. [ABSTRACT FROM AUTHOR]

Abstract Epigenetic processes manage gene expression and products in a real‐time manner, allowing a single genome to display different phenotypes. In this paper, we discussed the relevance of assessing the different sources of epigenetic variation in natural populations. For a given genotype, the epigenetic variation could be environmentally induced or occur randomly. Strategies developed by organisms to face environmental fluctuations such as phenotypic plasticity and diversified bet‐hedging rely, respectively, on these different sources. Random variation can also represent a proxy of developmental stability and can be used to assess how organisms deal with stressful environmental conditions. We then proposed the microbiome as an extension of the epigenotype of the host to assess the factors determining the establishment of the community of microorganisms. Finally, we discussed these perspectives in the applied context of conservation.

Abstract In this paper, we explore how two discrete and geographically separated populations of the lesser long‐nosed bat (Leptonycteris yerbabuenae)—one in central and the other in the Pacific region of Mexico—differ in their fecal microbiota composition. Considering the microbiota–host as a unity, in which extrinsic (as food availability and geography) or intrinsic factors (as physiology) play an important role in the microbiota composition, we would expect differentiation in the microbiota of two geographically separated populations. The Amplicon Sequences Variants (ASVs) of the V4 region of the 16s rRNA gene from 68 individuals were analyzed using alpha and beta diversity metrics. We obtained a total of 11 566 (ASVs). The bacterial communities in the Central and Pacific populations had a diversity of 6,939 and 4,088 ASVs, respectively, sharing a core microbiota of 539 ASVs accounting for 75% of the relative abundance, suggesting stability over evolutionary time. The Weighted UniFrac metrics tested by a PERMANOVA showed that lactating and pregnant females had significant beta diversity differences in the two populations compared with other reproductive stages. This could be a consequence of the increased energy requirements of these physiological stages, more than the variation due to geographical separation. In contrast, a positive correlation of the observed ASVs of fecal microbiota with the observed ASVs of plastids related to the diet was observed in the juveniles and adults, suggesting that in these physiological stages an extrinsic factor as the diet shapes the microbiota composition. The results provide a baseline for future studies of the microbiome in these two wild populations of the lesser long‐nosed bat, the main pollinator of the Agaves from which the beverages tequila and mezcal are made.

Tick-borne diseases, such as those transmitted by the blacklegged tick Ixodes scapularis, are a significant and growing public health problem in the US. There is mounting evidence that co-occurring non-pathogenic microbes can also impact tick-borne disease transmission. Shotgun metagenome sequencing enables sampling of the complete tick hologenome—the collective genomes of the tick and all of the microbial species contained therein, whether pathogenic, commensal or symbiotic. This approach simultaneously uncovers taxonomic composition and allows the detection of intraspecific genetic variation, making it a useful tool to compare spatial differences across tick populations. We evaluated this approach by comparing hologenome data from two tick samples (N = 6 ticks per location) collected at a relatively fine spatial scale, approximately 23 km apart, within a single US county. Several intriguing variants in the data between the two sites were detected, including polymorphisms in both in the tick’s own mitochondrial DNA and that of a rickettsial endosymbiont. The two samples were broadly similar in terms of the microbial species present, including multiple known tick-borne pathogens (Borrelia burgdorferi, Babesia microti, and Anaplasma phagocytophilum), filarial nematodes, and Wolbachia and Babesia species.We assembled the complete genome of the rickettsial endosymbiont (most likely Rickettsia buchneri) from both populations. Our results provide further evidence for the use of shotgun metagenome sequencing as a tool to compare tick hologenomes and differentiate tick populations across localized spatial scales. [ABSTRACT FROM AUTHOR]

Dietary changes can alter the human microbiome with potential detrimental consequences for health. Given that environment, health, and evolution are interconnected, we ask: Could diet‐driven microbiome perturbations have consequences that extend beyond their immediate impact on human health? We address this question in the context of the urgent health challenges posed by global climate change. Drawing on recent studies, we propose that not only can diet‐driven microbiome changes lead to dysbiosis, they can also shape life‐history traits and fuel human evolution. We posit that dietary shifts prompt mismatched microbiome‐host genetics configurations that modulate human longevity and reproductive success. These mismatches can also induce a heritable intra‐holobiont stress response, which encourages the holobiont to re‐establish equilibrium within the changed nutritional environment. Thus, while mismatches between climate change‐related genetic and epigenetic configurations within the holobiont increase the risk and severity of diseases, they may also affect life‐history traits and facilitate adaptive responses. These propositions form a framework that can help systematize and address climate‐related dietary challenges for policy and health interventions. [ABSTRACT FROM AUTHOR]

The concept of superorganism has a mixed reputation in biology—for some it is a convenient way of discussing supra-organismal levels of organization, and for others, little more than a poetic metaphor. Here, I show that a considerable step forward in the understanding of superorganisms results from a thorough review of the supra-organismal levels of organization now known to exist among the "unicellular" protists. Limiting the discussion to protists has enormous advantages: their bodies are very well studied and relatively simple (as compared to humans or termites, two standard examples in most discussions about superorganisms), and they exhibit an enormous diversity of anatomies and lifestyles. This allows for unprecedented resolution in describing forms of supra-organismal organization. Here, four criteria are used to differentiate loose, incidental associations of hosts with their microbiota from "actual" superorganisms: (1) obligatory character, (2) specific spatial localization of microbiota, (3) presence of attachment structures and (4) signs of co-evolution in phylogenetic analyses. Three groups—that have never before been described in the philosophical literature—merit special attention: Symbiontida (also called Postgaardea), Oxymonadida and Parabasalia. Specifically, it is argued that in certain cases—for Bihospites bacati and Calkinsia aureus (symbiontids), Streblomastix strix (an oxymonad), Joenia annectens and Mixotricha paradoxa (parabasalids) and Kentrophoros (a ciliate)—it is fully appropriate to describe the whole protist-microbiota assocation as a single organism ("superorganism") and its elements as "tissues" or, arguably, even "organs". To account for this level of biological complexity, I propose the term "structured superorganism". [ABSTRACT FROM AUTHOR]

In natural environments, microbial communities must constantly adapt to stressful environmental conditions. The genetic and phenotypic mechanisms underlying the adaptive response of microbial communities to new (and often complex) environments can be tackled with a combination of experimental evolution and next generation sequencing. This combination allows to analyse the real-time evolution of microbial populations in response to imposed environmental factors or during the interaction with a host, by screening for phenotypic and genotypic changes over a multitude of identical experimental cycles. Experimental evolution (EE) coupled with comparative genomics has indeed facilitated the monitoring of bacterial genetic evolution and the understanding of adaptive evolution processes. Basically, EE studies had long been done on single strains, allowing to reveal the dynamics and genetic targets of natural selection and to uncover the correlation between genetic and phenotypic adaptive changes. However, species are always evolving in relation with other species and have to adapt not only to the environment itself but also to the biotic environment dynamically shaped by the other species. Nowadays, there is a growing interest to apply EE on microbial communities evolving under natural environments. In this paper, we provide a non-exhaustive review of microbial EE studies done with systems of increasing complexity (from single species, to synthetic communities and natural communities) and with a particular focus on studies between plants and plant-associated microorganisms. We highlight some of the mechanisms controlling the functioning of microbial species and their adaptive responses to environment changes and emphasize the importance of considering bacterial communities and complex environments in EE studies.

Plants exist in close association with uncountable numbers of microorganisms around, on, and within them. Some of these endophytically colonize plant roots. The colonization of roots by certain symbiotic strains of plant-associated bacteria and fungi results in these plants performing better than plants whose roots are colonized by only the wild populations of microbes. We consider here crop plants whose roots are inhabited by introduced organisms, referring to them as Enhanced Plant Holobionts (EPHs). EPHs frequently exhibit resistance to specific plant diseases and pests (biotic stresses); resistance to abiotic stresses such as drought, cold, salinity, and flooding; enhanced nutrient acquisition and nutrient use efficiency; increased photosynthetic capability; and enhanced ability to maintain efficient internal cellular functioning. The microbes described here generate effects in part through their production of Symbiont-Associated Molecular Patterns (SAMPs) that interact with receptors in plant cell membranes. Such interaction results in the transduction of systemic signals that cause plant-wide changes in the plants' gene expression and physiology. EPH effects arise not only from plant-microbe interactions, but also from microbe-microbe interactions like competition, mycoparasitism, and antibiotic production. When root and shoot growth are enhanced as a consequence of these root endophytes, this increases the yield from EPH plants. An additional benefit from growing larger root systems and having greater photosynthetic capability is greater sequestration of atmospheric CO2. This is transferred to roots where sequestered C, through exudation or root decomposition, becomes part of the total soil carbon, which reduces global warming potential in the atmosphere. Forming EPHs requires selection and introduction of appropriate strains of microorganisms, with EPH performance affected also by the delivery and management practices. [ABSTRACT FROM AUTHOR]

According to a shared functionalist view in philosophy of mind, a cognitive system, and cognitive function thereof, is based on the components of the organism it is realized by which, indeed, play a causal role in regulating our cognitive processes. This led philosophers to suggest also that, thus, cognition could be seen as an extended process, whose vehicle can extend not only outside the brain but also beyond bodily boundaries, on different kinds of devices. This is what we call the ‘Externally Extended Cognition Thesis.’ This notion has generated a lively debate. Here, we offer a novel notion of extended cognition, according to which cognition can be seen as being realized (and expanded) outside the brain, but still inside the body. This is what we call the ‘Internally Extended Cognition Thesis’. Not only our thesis but also our approach while defending it is innovative. The argument we offer is supported by recent empirical findings in the life sciences and biomedicine, which suggest that the gut microbiota’s activity has a functional role in regulating our cognitive processes and behaviors. In doing so, we embrace the holobiont-perspective, according to which it is possible to claim that what we call biological individuals are not autonomous entities with clear boundaries, but should rather be seen as networks of multiple interactions among species. Thus, by analyzing different sets of evidence in light of the holobiont-perspective, we argue that the gut microbiota could be seen as a component of our organism. On the basis of the philosophical interpretation of this evidence, however, we also suggest that there are no impediments standing the way of considering the gut microbiota also as a functional extension of our cognitive system. If so, this amounts to extending cognition out of ‘our skull’, though still confining it within ‘our body’: to ‘our gut’. This is an instance of the ‘Internally Extended Cognition Thesis,’ whose benefits for an original (biologically informed) theory of extended cognition are discussed. [ABSTRACT FROM AUTHOR]

Aims: Phytoremediation of soil contaminated by trace elements is a technology using plants and microorganisms to sequester, inactivate, or extract contaminants from the soil. The assemblage formed by the partnership between plants and microorganisms is referred to as the plant holobiont concept. Among holobiont microorganisms, endophytes are associated with the plant at its earliest growth stage and are localized inside plant tissues. While plant tissues shelter endophytic microbial communities, mutualistic endophytes have shown a potential for plant growth promotion that will deeply and durably benefit the plant holobiont. In this review, we describe the state-of-the-art knowledge of the endophytes' role in plant growth promotion and the prospects for phytoremediation technologies. Results: Mutualistic symbionts have been demonstrated to improve plant growth, germination and yield. Indeed, they improve plant nutrition, increase plant resistance to bio-aggressors and stimulate plant metabolite productions. Research has shown that endophytes improve plant performance especially under extreme conditions such as drought, nitrogen deficiency, salinity and exposition to metal phytotoxicity. Endophyte inoculation has shown potential for plant growth promotion and has increased metal translocation in hyperaccumulator shoots by mitigating stresses from contaminated and naturally metal-rich soils. Conclusions: Endophytes have demonstrated their potential to enhance the plant's physiological status under metallic stress, the growth of both roots and shoots, as well as increasing metal uptake in the shoot biomass of a wide diversity of hyperaccumulating plants. Endophyte-assisted phytoremediation is a promising technology for the remediation of polluted or naturally metal-rich soils. [ABSTRACT FROM AUTHOR]

I address the question of how we should understand the holobiont and offer to look at it from the perspective of interactions. The debate about the holobiont centers on two issues: where to place its boundaries and what are the criteria for distinguishing inside from outside. By shifting the focus from degrees of cohesion of the host-symbiont interactions to the heterogeneity of interactions, I suggest a different perspective on interactions and their role in shaping the interacting agent (e.g., host-organism/microorganism/holobiont). I focus on the notion of mutuality of interactions by thinking about the holobiont through microbial interactions, using the case study of quorum sensing between bacterial cells. I conceptualize interactions as constitutive, placed on a scale between constitutive and contextual of each interacting agent. Constitutive interactions in this view are not interactions between individuals composing a third individual (i.e., symbionts within a host organism). Instead, the interactions are constitutive of each of the interacting organisms in interdependence relations. Furthermore, I argue that this interdependence involves the environment as an active participant which affects the nature of the interactions through environmental modifications. [ABSTRACT FROM AUTHOR]

The mechanical and chemical properties of natural plant fibers are determined by many different factors, both intrinsic and extrinsic to the plant, during growth but also after harvest. A better understanding of how all these factors exert their effect and how they interact is necessary to be able to optimize fiber quality for use in different industries. One important factor is the post-harvest process known as retting, representing the first step in the extraction of bast fibers from the stem of species such as flax and hemp. During this process microorganisms colonize the stem and produce hydrolytic enzymes that target cell wall polymers thereby facilitating the progressive destruction of the stem and fiber bundles. Recent advances in sequencing technology have allowed researchers to implement targeted metagenomics leading to a much better characterization of the microbial communities involved in retting, as well as an improved understanding of microbial dynamics. In this paper we review how our current knowledge of the microbiology of retting has been improved by targeted metagenomics and discuss how related ‘-omics’ approaches might be used to fully characterize the functional capability of the retting microbiome.

Microbiomes are transmitted between generations by a variety of different vertical and/or horizontal modes, including vegetative reproduction (vertical), via female germ cells (vertical), coprophagy and regurgitation (vertical and horizontal), physical contact starting at birth (vertical and horizontal), breast-feeding (vertical), and via the environment (horizontal). Analyses of vertical transmission can result in false negatives (failure to detect rare microbes) and false positives (strain variants). In humans, offspring receive most of their initial gut microbiota vertically from mothers during birth, via breast-feeding and close contact. Horizontal transmission is common in marine organisms and involves selectivity in determining which environmental microbes can colonize the organism’s microbiome. The following arguments are put forth concerning accurate microbial transmission: First, the transmission may be of functions, not necessarily of species; second, horizontal transmission may be as accurate as vertical transmission; third, detection techniques may fail to detect rare microbes; lastly, microbiomes develop and reach maturity with their hosts. In spite of the great variation in means of transmission discussed in this paper, microbiomes and their functions are transferred from one generation of holobionts to the next with fidelity. This provides a strong basis for each holobiont to be considered a unique biological entity and a level of selection in evolution, largely maintaining the uniqueness of the entity and conserving the species from one generation to the next.

Close reciprocal interactions in symbiotic systems have suggested the holobiont concept, in which the host and its microbiota are considered as a single entity. Ciliates are known for their ability to form symbiotic associations with prokaryotes. Relationships between the partners in such systems vary from mutualism to parasitism and differ significantly in their robustness. We assessed the viability of the ciliate Paramecium multimicronucleatum and its ability to maintain its intranuclear endosymbiont Ca. Trichorickettsia mobilis (Rickettsiaceae) after treatment with antibiotics characterized by different mode of action, such as ampicillin, streptomycin, chloramphenicol, tetracycline. The presence of endosymbionts in the host cell was determined by means of living cell observations made using differential interference contrast or fluorescence in situ hybridization with the species-specific oligonucleotide probe (FISH). Administration of antibiotics traditionally used in treatments of rickettsioses, tetracycline and chloramphenicol, depending on the concentration used and the ciliate strain treated, either caused death of both, infected and control cells, or did not affect the ability of the host to maintain the intranuclear endosymbiont. The surviving cells always manifested motile bacteria in the macronucleus. Streptomycin treatment never led to the loss of endosymbionts in any of the four infected strains, and nearly all ciliates remained viable. Ampicillin treatment never caused host cell death, but resulted in formation of filamentous and immobile oval bacterial forms. Under repeated ampicillin treatments, a part of endosymbionts was registered in the host cytoplasm, as evidenced both by FISH and transmission electron microscopy. Endosymbionts located in the host cytoplasm were enclosed in vacuoles, apparently, corresponding to autophagosomes. Nevertheless, the bacteria seemed to persist in this compartment and might cause relapse of the infection. Although the antibiotic sensitivity profile of Trichorickettsia seems to resemble that of other representatives of Rickettsiaceae, causative agents of severe diseases in humans, neither of the antibiotic treatments used in this study resulted in an aposymbiotic cell line, apparently, due to the protists' sensitivity to tetracyclines, the drugs of preference in rickettsiosis treatment. The observed robustness of this symbiotic system makes it a good model for further elaboration of the holobiont concept. [ABSTRACT FROM AUTHOR]

The recent explosive increase in the number of works on gut microbiota has been accompanied by the spread of rather vague or improper definitions, chosen more for common use than for experimental evidence. Among them are those defining the human gut microbiota as an organ of our body or as a commensal. But, is the human gut microbiota an organ or a commensal? Here, we address this issue to spearhead a reflection on the real roles of the human gut microbiota in our life. Actually, the misuse of the vocabulary used to describe the properties and functions of the gut microbiota may generate confusion and cause misunderstandings both in the scientific community and among the general public. [ABSTRACT FROM AUTHOR]

Given one conception of biological individuality (evolutionary, physiological, etc.), can a holobiont – that is the host + its symbiotic (mutualistic, commensalist and parasitic) microbiome – be simultaneously a biological individual and an ecological community? Herein, we support this possibility by arguing that the notion of biological individuality is part‐dependent. In our account, the individuality of a biological ensemble should not only be determined by the conception of biological individuality in use, but also by the biological characteristics of the part of the ensemble under investigation. In the specific case of holobionts, evaluations of their individuality should be made either host‐relative or microbe‐relative. We support the claim that biological individuality is part‐dependent by drawing upon recent empirical evidence regarding the physiology of hosts and microbes, and the recent characterization of the 'demibiont'. Our account shows that contemporary disagreements about the individuality of the holobiont derive from an incorrect understanding of the ontology of biological individuality. We show that collaboration between philosophers and biologists can be very fruitful in attempts to solve some contemporary biological debates. [ABSTRACT FROM AUTHOR]

Microorganismal diversity can be explained in large part by selection imposed from both the abiotic and biotic environments, including--in the case of host-associated microbiomes--interactions with eukaryotes. As such, the diversity of host-associated microbiomes can be usefully studied across a variety of scales: within a single host over time, among host genotypes within a population, between populations and among host species. A plethora of recent studies across these scales and across diverse systems are: (i) exemplifying the importance of the host genetics in shaping microbiome composition; (ii) uncovering the role of the microbiome in shaping key host phenotypes; and (iii) highlighting the dynamic nature of the microbiome. They have also raised a critical question: do these complex associations fit within our existing understanding of evolution and coevolution, or do these often intimate and seemingly cross-generational interactions follow novel evolutionary rules from those previously identified? Herein, we describe the known importance of (co)evolution in host-microbiome systems, placing the existing data within extant frameworks that have been developed over decades of study, and ask whether there are unique properties of host-microbiome systems that require a paradigm shift. By examining when and how selection can act on the host and its microbiome as a unit (termed, the holobiont), we find that the existing conceptual framework, which focuses on individuals, as well as interactions among individuals and groups, is generally well suited for understanding (co)evolutionary change in these intimate assemblages. This article is part of the theme issue 'The role of the microbiome in host evolution'. [ABSTRACT FROM AUTHOR]

This review explores how microbial symbioses may have influenced and continue to influence the evolution of reef-building corals (Cnidaria; Scleractinia). The coral holobiont comprises a diverse microbiome including dinoflagellate algae (Dinophyceae; Symbiodiniaceae), bacteria, archaea, fungi and viruses, but here we focus on the Symbiodiniaceae as knowledge of the impact of other microbial symbionts on coral evolution is scant. Symbiosis with Symbiodiniaceae has extended the coral's metabolic capacity through metabolic handoffs and horizontal gene transfer (HGT) and has contributed to the ecological success of these iconic organisms. It necessitated the prior existence or the evolution of a series of adaptations of the host to attract and select the right symbionts, to provide them with a suitable environment and to remove disfunctional symbionts. Signatures of microbial symbiosis in the coral genome include HGT from Symbiodiniaceae and bacteria, gene family expansions, and a broad repertoire of oxidative stress response and innate immunity genes. Symbiosis with Symbiodiniaceae has permitted corals to occupy oligotrophic waters as the algae provide most corals with the majority of their nutrition. However, the coral-Symbiodiniaceae symbiosis is sensitive to climate warming, which disrupts this intimate relationship, causing coral bleaching, mortality and a worldwide decline of coral reefs. This article is part of the theme issue 'The role of the microbiome in host evolution'. [ABSTRACT FROM AUTHOR]

An adequate account of how inferences and discoveries are made in modern biology is a difficult prospect for a philosopher. Do we really deduce conclusions from Darwin's principles? Once Darwinian biology is integrated with molecular biology, can we deduce the organism from its DNA? What does induction look like in an era where data sets are often too large to be processed by a human being? What is the role of abductive explanatory claims that try to define the biological individual in relation to the microbiome with which it may be associated, or to revise the notion of evolution when the interaction of organism and environment comes to seem much more complex than earlier generations imagined. How should we evaluate "origins of life" experiments conducted in the laboratory, where chemistry shifts to biology and we try to recreate early conditions on earth to which we have no empirical access? How are the carefully controlled conditions in the lab to be brought into productive relationship with the messy, contingent outdoor work of biologists in the field, studying crabs or eelgrass at the edge of the Pacific Ocean, or prairie plants at the end of woods, on the plains of the Midwest. To answer these questions, I sent my graduate student Tano Posteraro to work with Ted Grosholz, a marine biologist at the University of California / Davis, and my undergraduate student Alex Grigas to work with Ruth Geyer Shaw, a population geneticist at the University of Minnesota. They came back with complex and interesting answers to these questions. [ABSTRACT FROM AUTHOR]

Accurate delimitation of species and their relationships is a fundamental issue in evolutionary biology and taxonomy and provides essential implications for conservation management. Scleractinian corals are difficult to identify because of their ecophenotypic and geographic variation and their morphological plasticity. Furthermore, phylogenies based on traditional loci are often unresolved at the species level because of uninformative loci. Here, we attempted to resolve these issues and proposed a consistent species definition method for corals by applying the genome-wide technique Restriction-site Associated DNA sequencing (RADseq) to investigate phylogenetic relationships and species delimitation within the genus Leptastrea. We collected 77 colonies from nine localities of the Indo-Pacific and subjected them to genomic analyses. Based on de novo clustering, we obtained 44,162 SNPs (3701 loci) from the holobiont dataset and 62,728 SNPs (9573 loci) from the reads that map to coral transcriptome to reconstruct a robust phylogenetic hypothesis of the genus. Moreover, nearly complete mitochondrial genomes and ribosomal DNA arrays were retrieved by reference mapping. We combined concatenation-based phylogenetic analyses with coalescent-based species tree and species delimitation methods. Phylogenies suggest the presence of six distinct species, three corresponding to known taxa, namely Leptastrea bottae, Leptastrea inaequalis, Leptastrea transversa, one characterized by a remarkable skeletal variability encompassing the typical morphologies of Leptastrea purpurea and Leptastrea pruinosa, and two distinct and currently undescribed species. Therefore, based on the combination of genomic, morphological, morphometric, and distributional data, we herein described Leptastrea gibbosa sp. n. from the Pacific Ocean and Leptastrea magaloni sp. n. from the southwestern Indian Ocean and formally considered L. pruinosa as a junior synonym of L. purpurea. Notably, mitogenomes and rDNA yielded a concordant yet less resolved phylogeny reconstruction compared to the ones based on SNPs. This aspect demonstrates the strength and utility of RADseq technology for disentangling species boundaries in closely related species and in a challenging group such as scleractinian corals. [ABSTRACT FROM AUTHOR]

Animals and plants are metaorganisms and associate with microbes that affect their physiology, stress tolerance, and fitness. Here the hypothesis that alteration of the microbiome may constitute a fast‐response mechanism to environmental change is examined. This is supported by recent reciprocal transplant experiments with reef corals, which have shown that their microbiome adapts to thermally variable habitats and changes over time when transplanted into different environments. Further, inoculation of corals with beneficial bacteria increases their stress tolerance. But corals differ in their ability to flexibly associate with different bacteria. How scales of microbiome flexibility may reflect different metaorganism adaptation mechanisms is discussed and future directions for research are pinpointed. It is posited that microbiome flexibility is a broad phenomenon that contributes to the ability of organisms to respond to environmental change. Importantly, adapting with microbial help may provide an alternate route to organismal adaptation that facilitates rapid responses. [ABSTRACT FROM AUTHOR]

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral-turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes. [ABSTRACT FROM AUTHOR]