De novo phytosterol synthesis in animals.

Sterols are vital for nearly all eukaryotes. Their distribution differs in plants and animals, with phytosterols commonly found in plants whereas most animals are dominated by cholesterol. We show that sitosterol, a common sterol of plants, is the most abundant sterol in gutless marine annelids. Using multiomics, metabolite imaging, heterologous gene expression, and enzyme assays, we show that these animals synthesize sitosterol de novo using a noncanonical C-24 sterol methyltransferase (C24-SMT). This enzyme is essential for sitosterol synthesis in plants, but not known from most bilaterian animals. Our phylogenetic analyses revealed that C24-SMTs are present in representatives of at least five animal phyla, indicating that the synthesis of sterols common to plants is more widespread in animals than currently known.

Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium.

BACKGROUND: Many animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species. RESULTS: In this study on the obligate symbiosis between the gutless marine annelid Olavius algarvensis and its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80 O. algarvensis individuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of all O. algarvensis individuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted. CONCLUSIONS: We hypothesize that variable degrees of fidelity are advantageous for O. algarvensis by allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources. Video Abstract.

Sugars dominate the seagrass rhizosphere.

Seagrasses are among the most efficient sinks of carbon dioxide on Earth. While carbon sequestration in terrestrial plants is linked to the microorganisms living in their soils, the interactions of seagrasses with their rhizospheres are poorly understood. Here, we show that the seagrass, Posidonia oceanica excretes sugars, mainly sucrose, into its rhizosphere. These sugars accumulate to µM concentrations-nearly 80 times higher than previously observed in marine environments. This finding is unexpected as sugars are readily consumed by microorganisms. Our experiments indicated that under low oxygen conditions, phenolic compounds from P. oceanica inhibited microbial consumption of sucrose. Analyses of the rhizosphere community revealed that many microbes had the genes for degrading sucrose but these were only expressed by a few taxa that also expressed genes for degrading phenolics. Given that we observed high sucrose concentrations underneath three other species of marine plants, we predict that the presence of plant-produced phenolics under low oxygen conditions allows the accumulation of labile molecules across aquatic rhizospheres.

Life in the Dark: Phylogenetic and Physiological Diversity of Chemosynthetic Symbioses.

Possibly the last discovery of a previously unknown major ecosystem on Earth was made just over half a century ago, when researchers found teaming communities of animals flourishing two and a half kilometers below the ocean surface at hydrothermal vents. We now know that these highly productive ecosystems are based on nutritional symbioses between chemosynthetic bacteria and eukaryotes and that these chemosymbioses are ubiquitous in both deep-sea and shallow-water environments. The symbionts are primary producers that gain energy from the oxidation of reduced compounds, such as sulfide and methane, to fix carbon dioxide or methane into biomass to feed their hosts. This review outlines how the symbiotic partners have adapted to living together. We first focus on the phylogenetic and metabolic diversity of these symbioses and then highlight selected research directions that could advance our understanding of the processes that shaped the evolutionary and ecological success of these associations.

Coming together-symbiont acquisition and early development in deep-sea bathymodioline mussels.

How and when symbionts are acquired by their animal hosts has a profound impact on the ecology and evolution of the symbiosis. Understanding symbiont acquisition is particularly challenging in deep-sea organisms because early life stages are so rarely found. Here, we collected early developmental stages of three deep-sea bathymodioline species from different habitats to identify when these acquire their symbionts and how their body plan adapts to a symbiotic lifestyle. These mussels gain their nutrition from chemosynthetic bacteria, allowing them to thrive at deep-sea vents and seeps worldwide. Correlative imaging analyses using synchrotron-radiation based microtomography together with light, fluorescence and electron microscopy revealed that the pediveliger larvae were aposymbiotic. Symbiont colonization began during metamorphosis from a planktonic to a benthic lifestyle, with the symbionts rapidly colonizing first the gills, the symbiotic organ of adults, followed by all other epithelia of their hosts. Once symbiont densities in plantigrades reached those of adults, the host's intestine changed from the looped anatomy typical for bivalves to a straightened form. Within the Mytilidae, this morphological change appears to be specific to Bathymodiolus and Gigantidas, and is probably linked to the decrease in the importance of filter feeding when these mussels switch to gaining their nutrition largely from their symbionts.

Deep-sea mussels from a hybrid zone on the Mid-Atlantic Ridge host genetically indistinguishable symbionts.

The composition and diversity of animal microbiomes is shaped by a variety of factors, many of them interacting, such as host traits, the environment, and biogeography. Hybrid zones, in which the ranges of two host species meet and hybrids are found, provide natural experiments for determining the drivers of microbiome communities, but have not been well studied in marine environments. Here, we analysed the composition of the symbiont community in two deep-sea, Bathymodiolus mussel species along their known distribution range at hydrothermal vents on the Mid-Atlantic Ridge, with a focus on the hybrid zone where they interbreed. In-depth metagenomic analyses of the sulphur-oxidising symbionts of 30 mussels from the hybrid zone, at a resolution of single nucleotide polymorphism analyses of ~2500 orthologous genes, revealed that parental and hybrid mussels (F2-F4 generation) have genetically indistinguishable symbionts. While host genetics does not appear to affect symbiont composition in these mussels, redundancy analyses showed that geographic location of the mussels on the Mid-Atlantic Ridge explained most of the symbiont genetic variability compared to the other factors. We hypothesise that geographic structuring of the free-living symbiont population plays a major role in driving the composition of the microbiome in these deep-sea mussels.

Chemosynthetic symbioses.

Symbioses between chemosynthetic bacteria and eukaryotic hosts can be found almost everywhere in the ocean, from shallow-water seagrass beds and coral reef sediments to the deep sea. Yet no one knew these existed until 45 years ago, when teeming communities of animals were found thriving at hydrothermal vents two and a half kilometers below the sea surface. The discovery of these lightless ecosystems revolutionized our understanding of the energy sources that fuel life on Earth. Animals thrive at vents because they live in a nutritional symbiosis with chemosynthetic bacteria that grow on chemical compounds gushing out of the vents, such as sulfide and methane, which animals cannot use on their own. The symbionts gain energy from the oxidation of these reduced substrates to fix CO2 and other simple carbon compounds into biomass, which is then transferred to the host. By associating with chemosynthetic bacteria, animals and protists can thrive in environments in which there is not enough organic carbon to support their nutrition, including oligotrophic habitats like coral reefs and seagrass meadows. Chemosymbioses have evolved repeatedly and independently in multiple lineages of marine invertebrates and bacteria, highlighting the strong selective advantage for both hosts and symbionts in forming these associations. Here, we provide a brief overview of chemosynthesis and how these symbioses function. We highlight some of the current research in this field and outline several promising avenues for future research.

High-Quality Draft Genome Sequences of the Uncultured Delta3 Endosymbiont (Deltaproteobacteria) Assembled from Metagenomes of the Gutless Marine Worm Olavius algarvensis.

Here, we present two high-quality, draft metagenome-assembled genomes of deltaproteobacterial OalgDelta3 endosymbionts from the gutless marine worm Olavius algarvensis Their 16S rRNA gene sequences share 98% identity with Delta3 endosymbionts of related host species Olavius ilvae (GenBank accession no. AJ620501) and Inanidrilus exumae (GenBank accession no. FM202060), for which no symbiont genomes are available.

High-Quality Draft Genome Sequences of Two Deltaproteobacterial Endosymbionts, Delta1a and Delta1b, from the Uncultured Sva0081 Clade, Assembled from Metagenomes of the Gutless Marine Worm Olavius algarvensis.

Here, we present high-quality metagenome-assembled genome sequences of two closely related deltaproteobacterial endosymbionts from the gutless marine worm Olavius algarvensis (Annelida). The first is an improved draft genome sequence of the previously described sulfate-reducing symbiont Delta1. The second is from a closely related, recently discovered symbiont of O. algarvensis.

Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans.

BACKGROUND: Apicomplexans are the causative agents of major human diseases such as malaria and toxoplasmosis. A novel group of apicomplexans, recently named corallicolids, have been detected in corals inhabiting tropical shallow reefs. These apicomplexans may represent a transitional lifestyle between free-living phototrophs and obligate parasites. To shed light on the evolutionary history of apicomplexans and to investigate their ecology in association with corals, we screened scleractinians, antipatharians, alcyonaceans, and zoantharians from shallow, mesophotic, and deep-sea communities. We detected corallicolid plastids using 16S metabarcoding, sequenced the nuclear 18S rRNA gene of corallicolids from selected samples, assembled and annotated the plastid and mitochondrial genomes from a corallicolid that associates with a deep-sea coral, and screened the metagenomes of four coral species for corallicolids. RESULTS: We detected 23 corallicolid plastotypes that were associated with 14 coral species from three orders and depths down to 1400 m. Individual plastotypes were restricted to coral hosts within a single depth zone and within a single taxonomic order of corals. Some clusters of closely related corallicolids were revealed that associated with closely related coral species. However, the presence of divergent corallicolid lineages that associated with similar coral species and depths suggests that corallicolid/coral relations are flexible over evolutionary timescales and that a large diversity of apicomplexans may remain undiscovered. The corallicolid plastid genome from a deep-sea coral contained four genes involved in chlorophyll biosynthesis: the three genes of the LIPOR complex and acsF. CONCLUSIONS: The presence of corallicolid apicomplexans in corals below the photic zone demonstrates that they are not restricted to shallow-water reefs and are more general anthozoan symbionts. The presence of LIPOR genes in the deep-sea corallicolid precludes a role involving photosynthesis and suggests they may be involved in a different function. Thus, these genes may represent another set of genetic tools whose function was adapted from photosynthesis as the ancestors of apicomplexans evolved towards parasitic lifestyles. Video abstract.

Spatial metabolomics of in situ host-microbe interactions at the micrometre scale.

Spatial metabolomics describes the location and chemistry of small molecules involved in metabolic phenotypes, defence molecules and chemical interactions in natural communities. Most current techniques are unable to spatially link the genotype and metabolic phenotype of microorganisms in situ at a scale relevant to microbial interactions. Here, we present a spatial metabolomics pipeline (metaFISH) that combines fluorescence in situ hybridization (FISH) microscopy and high-resolution atmospheric-pressure matrix-assisted laser desorption/ionization mass spectrometry to image host-microbe symbioses and their metabolic interactions. The metaFISH pipeline aligns and integrates metabolite and fluorescent images at the micrometre scale to provide a spatial assignment of host and symbiont metabolites on the same tissue section. To illustrate the advantages of metaFISH, we mapped the spatial metabolome of a deep-sea mussel and its intracellular symbiotic bacteria at the scale of individual epithelial host cells. Our analytical pipeline revealed metabolic adaptations of the epithelial cells to the intracellular symbionts and variation in metabolic phenotypes within a single symbiont 16S rRNA phylotype, and enabled the discovery of specialized metabolites from the host-microbe interface. metaFISH provides a culture-independent approach to link metabolic phenotypes to community members in situ and is a powerful tool for microbiologists across fields.

Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria).

Most autotrophs use the Calvin-Benson-Bassham (CBB) cycle for carbon fixation. In contrast, all currently described autotrophs from the Campylobacterota (previously Epsilonproteobacteria) use the reductive tricarboxylic acid cycle (rTCA) instead. We discovered campylobacterotal epibionts ("Candidatus Thiobarba") of deep-sea mussels that have acquired a complete CBB cycle and may have lost most key genes of the rTCA cycle. Intriguingly, the phylogenies of campylobacterotal CBB cycle genes suggest they were acquired in multiple transfers from Gammaproteobacteria closely related to sulfur-oxidizing endosymbionts associated with the mussels, as well as from Betaproteobacteria. We hypothesize that "Ca. Thiobarba" switched from the rTCA cycle to a fully functional CBB cycle during its evolution, by acquiring genes from multiple sources, including co-occurring symbionts. We also found key CBB cycle genes in free-living Campylobacterota, suggesting that the CBB cycle may be more widespread in this phylum than previously known. Metatranscriptomics and metaproteomics confirmed high expression of CBB cycle genes in mussel-associated "Ca. Thiobarba". Direct stable isotope fingerprinting showed that "Ca. Thiobarba" has typical CBB signatures, suggesting that it uses this cycle for carbon fixation. Our discovery calls into question current assumptions about the distribution of carbon fixation pathways in microbial lineages, and the interpretation of stable isotope measurements in the environment.

Marine Metabolomics: a Method for Nontargeted Measurement of Metabolites in Seawater by Gas Chromatography-Mass Spectrometry.

Microbial communities exchange molecules with their environment, which plays a major role in regulating global biogeochemical cycles and climate. While extracellular metabolites are commonly measured in terrestrial and limnic ecosystems, the presence of salt in marine habitats limits the nontargeted analyses of the ocean exometabolome using mass spectrometry (MS). Current methods require salt removal prior to sample measurements, which can alter the molecular composition of the metabolome and limit the types of compounds detected by MS. To overcome these limitations, we developed a gas chromatography MS (GC-MS) method that avoids sample altering during salt removal and that detects metabolites down to nanomolar concentrations from less than 1 ml of seawater. We applied our method (SeaMet) to explore marine metabolomes in vitro and in vivo First, we measured the production and consumption of metabolites during the culture of a heterotrophic bacterium, Marinobacter adhaerens Our approach revealed successional uptake of amino acids, while sugars were not consumed. These results show that exocellular metabolomics provides insights into nutrient uptake and energy conservation in marine microorganisms. We also applied SeaMet to explore the in situ metabolome of coral reef and mangrove sediment porewaters. Despite the fact that these ecosystems occur in nutrient-poor waters, we uncovered high concentrations of sugars and fatty acids, compounds predicted to play a key role for the abundant and diverse microbial communities in coral reef and mangrove sediments. Our data demonstrate that SeaMet advances marine metabolomics by enabling a nontargeted and quantitative analysis of marine metabolites, thus providing new insights into nutrient cycles in the oceans.IMPORTANCE Nontargeted approaches using metabolomics to analyze metabolites that occur in the oceans is less developed than those for terrestrial and limnic ecosystems. One of the challenges in marine metabolomics is that salt limits metabolite analysis in seawater to methods requiring salt removal. Building on previous sample preparation methods for metabolomics, we developed SeaMet, which overcomes the limitations of salt on metabolite detection. Considering that the oceans contain the largest dissolved organic matter pool on Earth, describing the marine metabolome using nontargeted approaches is critical for understanding the drivers behind element cycles, biotic interactions, ecosystem function, and atmospheric CO2 storage. Our method complements both targeted marine metabolomic investigations as well as other "omics" (e.g., genomics, transcriptomics, and proteomics) approaches by providing an avenue for studying the chemical interaction between marine microbes and their habitats.

Functional diversity enables multiple symbiont strains to coexist in deep-sea mussels.

Genetic diversity of closely related free-living microorganisms is widespread and underpins ecosystem functioning, but most evolutionary theories predict that it destabilizes intimate mutualisms. Accordingly, strain diversity is assumed to be highly restricted in intracellular bacteria associated with animals. Here, we sequenced metagenomes and metatranscriptomes of 18 Bathymodiolus mussel individuals from four species, covering their known distribution range at deep-sea hydrothermal vents in the Atlantic. We show that as many as 16 strains of intracellular, sulfur-oxidizing symbionts coexist in individual Bathymodiolus mussels. Co-occurring symbiont strains differed extensively in key functions, such as the use of energy and nutrient sources, electron acceptors and viral defence mechanisms. Most strain-specific genes were expressed, highlighting their potential to affect fitness. We show that fine-scale diversity is pervasive in Bathymodiolus sulfur-oxidizing symbionts, and hypothesize that it may be widespread in low-cost symbioses where the environment, rather than the host, feeds the symbionts.

Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated.

Eukaryotes are habitats for bacterial organisms where the host colonization and dispersal among individual hosts have consequences for the bacterial ecology and evolution. Vertical symbiont transmission leads to geographic isolation of the microbial population and consequently to genetic isolation of microbiotas from individual hosts. In contrast, the extent of geographic and genetic isolation of horizontally transmitted microbiota is poorly characterized. Here we show that chemosynthetic symbionts of individual Bathymodiolus brooksi mussels constitute genetically isolated subpopulations. The reconstruction of core genome-wide strains from high-resolution metagenomes revealed distinct phylogenetic clades. Nucleotide diversity and strain composition vary along the mussel life span and individual hosts show a high degree of genetic isolation. Our results suggest that the uptake of environmental bacteria is a restricted process in B. brooksi, where self-infection of the gill tissue results in serial founder effects during symbiont evolution. We conclude that bacterial colonization dynamics over the host life cycle is thus an important determinant of population structure and genome evolution of horizontally transmitted symbionts.

Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO2 Fixation.

Since the discovery of symbioses between sulfur-oxidizing (thiotrophic) bacteria and invertebrates at hydrothermal vents over 40 years ago, it has been assumed that autotrophic fixation of CO2 by the symbionts drives these nutritional associations. In this study, we investigated "Candidatus Kentron," the clade of symbionts hosted by Kentrophoros, a diverse genus of ciliates which are found in marine coastal sediments around the world. Despite being the main food source for their hosts, Kentron bacteria lack the key canonical genes for any of the known pathways for autotrophic carbon fixation and have a carbon stable isotope fingerprint that is unlike other thiotrophic symbionts from similar habitats. Our genomic and transcriptomic analyses instead found metabolic features consistent with growth on organic carbon, especially organic and amino acids, for which they have abundant uptake transporters. All known thiotrophic symbionts have converged on using reduced sulfur to gain energy lithotrophically, but they are diverse in their carbon sources. Some clades are obligate autotrophs, while many are mixotrophs that can supplement autotrophic carbon fixation with heterotrophic capabilities similar to those in Kentron. Here we show that Kentron bacteria are the only thiotrophic symbionts that appear to be entirely heterotrophic, unlike all other thiotrophic symbionts studied to date, which possess either the Calvin-Benson-Bassham or the reverse tricarboxylic acid cycle for autotrophy.IMPORTANCE Many animals and protists depend on symbiotic sulfur-oxidizing bacteria as their main food source. These bacteria use energy from oxidizing inorganic sulfur compounds to make biomass autotrophically from CO2, serving as primary producers for their hosts. Here we describe a clade of nonautotrophic sulfur-oxidizing symbionts, "Candidatus Kentron," associated with marine ciliates. They lack genes for known autotrophic pathways and have a carbon stable isotope fingerprint heavier than other symbionts from similar habitats. Instead, they have the potential to oxidize sulfur to fuel the uptake of organic compounds for heterotrophic growth, a metabolic mode called chemolithoheterotrophy that is not found in other symbioses. Although several symbionts have heterotrophic features to supplement primary production, in Kentron they appear to supplant it entirely.

Two intracellular and cell type-specific bacterial symbionts in the placozoan Trichoplax H2.

Placozoa is an enigmatic phylum of simple, microscopic, marine metazoans1,2. Although intracellular bacteria have been found in all members of this phylum, almost nothing is known about their identity, location and interactions with their host3-6. We used metagenomic and metatranscriptomic sequencing of single host individuals, plus metaproteomic and imaging analyses, to show that the placozoan Trichoplax sp. H2 lives in symbiosis with two intracellular bacteria. One symbiont forms an undescribed genus in the Midichloriaceae (Rickettsiales)7,8 and has a genomic repertoire similar to that of rickettsial parasites9,10, but does not seem to express key genes for energy parasitism. Correlative image analyses and three-dimensional electron tomography revealed that this symbiont resides in the rough endoplasmic reticulum of its host's internal fibre cells. The second symbiont belongs to the Margulisbacteria, a phylum without cultured representatives and not known to form intracellular associations11-13. This symbiont lives in the ventral epithelial cells of Trichoplax, probably metabolizes algal lipids digested by its host and has the capacity to supplement the placozoan's nutrition. Our study shows that one of the simplest animals has evolved highly specific and intimate associations with symbiotic, intracellular bacteria and highlights that symbioses can provide access to otherwise elusive microbial dark matter.

Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts.

Sponges host a remarkable diversity of microbial symbionts, however, the benefit their microbes provide is rarely understood. Here, we describe two new sponge species from deep-sea asphalt seeps and show that they live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria. Metagenomics and imaging analyses revealed unusually high amounts of MOX symbionts in hosts from a group previously assumed to have low microbial abundances. These symbionts belonged to the Marine Methylotrophic Group 2 clade. They are host-specific and likely vertically transmitted, based on their presence in sponge embryos and streamlined genomes, which lacked genes typical of related free-living MOX. Moreover, genes known to play a role in host-symbiont interactions, such as those that encode eukaryote-like proteins, were abundant and expressed. Methane assimilation by the symbionts was one of the most highly expressed metabolic pathways in the sponges. Molecular and stable carbon isotope patterns of lipids confirmed that methane-derived carbon was incorporated into the hosts. Our results revealed that two species of sponges, although distantly related, independently established highly specific, nutritional symbioses with two closely related methanotrophs. This convergence in symbiont acquisition underscores the strong selective advantage for these sponges in harboring MOX bacteria in the food-limited deep sea.

Genetic Evidence for Two Carbon Fixation Pathways (the Calvin-Benson-Bassham Cycle and the Reverse Tricarboxylic Acid Cycle) in Symbiotic and Free-Living Bacteria.

Very few bacteria are able to fix carbon via both the reverse tricarboxylic acid (rTCA) and the Calvin-Benson-Bassham (CBB) cycles, such as symbiotic, sulfur-oxidizing bacteria that are the sole carbon source for the marine tubeworm Riftia pachyptila, the fastest-growing invertebrate. To date, the coexistence of these two carbon fixation pathways had not been found in a cultured bacterium and could thus not be studied in detail. Moreover, it was not clear if these two pathways were encoded in the same symbiont individual, or if two symbiont populations, each with one of the pathways, coexisted within tubeworms. With comparative genomics, we show that Thioflavicoccus mobilis, a cultured, free-living gammaproteobacterial sulfur oxidizer, possesses the genes for both carbon fixation pathways. Here, we also show that both the CBB and rTCA pathways are likely encoded in the genome of the sulfur-oxidizing symbiont of the tubeworm Escarpia laminata from deep-sea asphalt volcanoes in the Gulf of Mexico. Finally, we provide genomic and transcriptomic data suggesting a potential electron flow toward the rTCA cycle carboxylase 2-oxoglutarate:ferredoxin oxidoreductase, via a rare variant of NADH dehydrogenase/heterodisulfide reductase in the E. laminata symbiont. This electron-bifurcating complex, together with NAD(P)+ transhydrogenase and Na+ translocating Rnf membrane complexes, may improve the efficiency of the rTCA cycle in both the symbiotic and the free-living sulfur oxidizer.IMPORTANCE Primary production on Earth is dependent on autotrophic carbon fixation, which leads to the incorporation of carbon dioxide into biomass. Multiple metabolic pathways have been described for autotrophic carbon fixation, but most autotrophic organisms were assumed to have the genes for only one of these pathways. Our finding of a cultivable bacterium with two carbon fixation pathways in its genome, the rTCA and the CBB cycle, opens the possibility to study the potential benefits of having these two pathways and the interplay between them. Additionally, this will allow the investigation of the unusual and potentially very efficient mechanism of electron flow that could drive the rTCA cycle in these autotrophs. Such studies will deepen our understanding of carbon fixation pathways and could provide new avenues for optimizing carbon fixation in biotechnological applications.

Metaorganisms in extreme environments: do microbes play a role in organismal adaptation?

From protists to humans, all animals and plants are inhabited by microbial organisms. There is an increasing appreciation that these resident microbes influence the fitness of their plant and animal hosts, ultimately forming a metaorganism consisting of a uni- or multicellular host and a community of associated microorganisms. Research on host-microbe interactions has become an emerging cross-disciplinary field. In both vertebrates and invertebrates a complex microbiome confers immunological, metabolic and behavioural benefits; conversely, its disturbance can contribute to the development of disease states. However, the molecular and cellular mechanisms controlling the interactions within a metaorganism are poorly understood and many key interactions between the associated organisms remain unknown. In this perspective article, we outline some of the issues in interspecies interactions and in particular address the question of how metaorganisms react and adapt to inputs from extreme environments such as deserts, the intertidal zone, oligothrophic seas, and hydrothermal vents.