Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective.

Microplastics have emerged as a significant global concern, particularly in marine ecosystems. While extensive research has focused on the toxicological effects of microplastics on marine animals and/or their associated microorganisms as two separate entities, the holistic perspective of the adaptability and fitness of a marine animal metaorganism-comprising the animal host and its microbiome-remains largely unexplored. In this study, mussel metaorganisms subjected chronic PS-MPs exposure experienced acute mortality but rapidly adapted. We investigated the response of innate immunity, digestive enzymes and their associated microbiomes to chronic PS-MPs exposure. We found that PS-MPs directly and indirectly interacted with the host and microbe within the exposure system. The adaptation was a joint effort between the physiological adjustments of mussel host and genetic adaptation of its microbiome. The mussel hosts exhibited increased antioxidant activity, denser gill filaments and increased immune cells, enhancing their innate immunity. Concurrently, the gill microbiome and the digestive gland microbiome respective selectively enriched for plastic-degrading bacteria and particulate organic matter-utilizing bacteria, facilitating the microbiome's adaptation. The microbial adaptation to chronic PS-MPs exposure altered the ecological roles of mussel microbiome, as evidenced by alterations in microbial interactions and nutrient cycling functions. These findings provided new insights into the ecotoxicological impact of microplastics on marine organisms from a metaorganism perspective.

The potential importance of the built-environment microbiome and its impact on human health.

There is increasing evidence that interactions between microbes and their hosts not only play a role in determining health and disease but also in emotions, thought, and behavior. Built environments greatly influence microbiome exposures because of their built-in highly specific microbiomes coproduced with myriad metaorganisms including humans, pets, plants, rodents, and insects. Seemingly static built structures host complex ecologies of microorganisms that are only starting to be mapped. These microbial ecologies of built environments are directly and interdependently affected by social, spatial, and technological norms. Advances in technology have made these organisms visible and forced the scientific community and architects to rethink gene-environment and microbe interactions respectively. Thus, built environment design must consider the microbiome, and research involving host-microbiome interaction must consider the built-environment. This paradigm shift becomes increasingly important as evidence grows that contemporary built environments are steadily reducing the microbial diversity essential for human health, well-being, and resilience while accelerating the symptoms of human chronic diseases including environmental allergies, and other more life-altering diseases. New models of design are required to balance maximizing exposure to microbial diversity while minimizing exposure to human-associated diseases. Sustained trans-disciplinary research across time (evolutionary, historical, and generational) and space (cultural and geographical) is needed to develop experimental design protocols that address multigenerational multispecies health and health equity in built environments.

The archaeome in metaorganism research, with a focus on marine models and their bacteria-archaea interactions.

Metaorganism research contributes substantially to our understanding of the interaction between microbes and their hosts, as well as their co-evolution. Most research is currently focused on the bacterial community, while archaea often remain at the sidelines of metaorganism-related research. Here, we describe the archaeome of a total of eleven classical and emerging multicellular model organisms across the phylogenetic tree of life. To determine the microbial community composition of each host, we utilized a combination of archaea and bacteria-specific 16S rRNA gene amplicons. Members of the two prokaryotic domains were described regarding their community composition, diversity, and richness in each multicellular host. Moreover, association with specific hosts and possible interaction partners between the bacterial and archaeal communities were determined for the marine models. Our data show that the archaeome in marine hosts predominantly consists of Nitrosopumilaceae and Nanoarchaeota, which represent keystone taxa among the porifera. The presence of an archaeome in the terrestrial hosts varies substantially. With respect to abundant archaeal taxa, they harbor a higher proportion of methanoarchaea over the aquatic environment. We find that the archaeal community is much less diverse than its bacterial counterpart. Archaeal amplicon sequence variants are usually host-specific, suggesting adaptation through co-evolution with the host. While bacterial richness was higher in the aquatic than the terrestrial hosts, a significant difference in diversity and richness between these groups could not be observed in the archaeal dataset. Our data show a large proportion of unclassifiable archaeal taxa, highlighting the need for improved cultivation efforts and expanded databases.

Marine bacteriophages disturb the associated microbiota of Aurelia aurita with a recoverable effect on host morphology.

The concept of the metaorganism describes a multicellular host and its diverse microbial community, which form one biological unit with a combined genetic repertoire that significantly influences health and survival of the host. The present study delved into the emerging field of bacteriophage research within metaorganisms, focusing on the moon jellyfish Aurelia aurita as a model organism. The previously isolated Pseudomonas phage BSwM KMM1 and Citrobacter phages BSwM KMM2 - KMM4 demonstrated potent infectivity on bacteria present in the A. aurita-associated microbiota. In a host-fitness experiment, Baltic Sea subpopulation polyps were exposed to individual phages and a phage cocktail, monitoring polyp survival and morphology, as well as microbiome changes. The following effects were obtained. First, phage exposure in general led to recoverable malformations in polyps without affecting their survival. Second, analyses of the community structure, using 16S rRNA amplicon sequencing, revealed alterations in the associated microbial community in response to phage exposure. Third, the native microbiota is dominated by an uncultured likely novel Mycoplasma species, potentially specific to A. aurita. Notably, this main colonizer showed resilience through the recovery after initial declines, which aligned with abundance changes in Bacteroidota and Proteobacteria, suggesting a dynamic and adaptable microbial community. Overall, this study demonstrates the resilience of the A. aurita metaorganism facing phage-induced perturbations, emphasizing the importance of understanding host-phage interactions in metaorganism biology. These findings have implications for ecological adaptation and conservation in the rapidly changing marine environment, particularly regarding the regulation of blooming species and the health of marine ecosystems during ongoing environmental changes.

The source of microbial transmission influences niche colonization and microbiome development.

Early life microbial colonizers shape and support the immature vertebrate immune system. Microbial colonization relies on the vertical route via parental provisioning and the horizontal route via environmental contribution. Vertical transmission is mostly a maternal trait making it hard to determine the source of microbial colonization in order to gain insight into the establishment of the microbial community during crucial development stages. The evolution of unique male pregnancy in pipefishes and seahorses enables the disentanglement of both horizontal and vertical transmission, but also facilitates the differentiation of maternal versus paternal provisioning ranging from egg development, to male pregnancy and early juvenile development. Using 16S rRNA amplicon sequencing and source-tracker analyses, we revealed how the distinct origins of transmission (maternal, paternal and horizontal) shaped the juvenile internal and external microbiome establishment in the broad-nosed pipefish Syngnathus typhle. Our data suggest that transovarial maternal microbial contribution influences the establishment of the juvenile gut microbiome whereas paternal provisioning mainly shapes the juvenile external microbiome. The identification of juvenile key microbes reveals crucial temporal shifts in microbial development and enhances our understanding of microbial transmission routes, colonization dynamics and their impact on lifestyle evolution.

The intricate triangular interaction between protective microbe, pathogen and host determines fitness of the metaorganism.

The microbiota shapes host biology in numerous ways. One example is protection against pathogens, which is likely critical for host fitness in consideration of the ubiquity of pathogens. The host itself can affect abundance of microbiota or pathogens, which has usually been characterized in separate studies. To date, however, it is unclear how the host influences the interaction with both simultaneously and how this triangular interaction determines fitness of the host-microbe assemblage, the so-called metaorganism. To address this current knowledge gap, we focused on a triangular model interaction, consisting of the nematode Caenorhabditis elegans, its protective symbiont Pseudomonas lurida MYb11 and its pathogen Bacillus thuringiensis Bt679. We combined the two microbes with C. elegans mutants with altered immunity and/or microbial colonization, and found that (i) under pathogen stress, immunocompetence has a larger influence on metaorganism fitness than colonization with the protective microbe; (ii) in almost all cases, MYb11 still improves fitness; and (iii) disruption of p38 MAPK signalling, which contributes centrally to immunity against Bt679, completely reverses the protective effect of MYb11, which further reduces nematode survival and fitness upon infection with Bt679. Our study highlights the complex interplay between host, protective microbe and pathogen in shaping metaorganism biology.

Microbial community changes correlate with impaired host fitness of Aurelia aurita after environmental challenge.

Climate change globally endangers certain marine species, but at the same time, such changes may promote species that can tolerate and adapt to varying environmental conditions. Such acclimatization can be accompanied or possibly even be enabled by a host's microbiome; however, few studies have so far directly addressed this process. Here we show that acute, individual rises in seawater temperature and salinity to sub-lethal levels diminished host fitness of the benthic Aurelia aurita polyp, demonstrated by up to 34% reduced survival rate, shrinking of the animals, and almost halted asexual reproduction. Changes in the fitness of the polyps to environmental stressors coincided with microbiome changes, mainly within the phyla Proteobacteria and Bacteroidota. The absence of bacteria amplified these effects, pointing to the benefit of a balanced microbiota to cope with a changing environment. In a future ocean scenario, mimicked by a combined but milder rise of temperature and salinity, the fitness of polyps was severely less impaired, together with condition-specific changes in the microbiome composition. Our results show that the effects on host fitness correlate with the strength of environmental stress, while salt-conveyed thermotolerance might be involved. Further, a specific, balanced microbiome of A. aurita polyps supports the host's acclimatization. Microbiomes may provide a means for acclimatization, and microbiome flexibility can be a fundamental strategy for marine animals to adapt to future ocean scenarios and maintain biodiversity and ecosystem functioning.

Co-evolution within the plant holobiont drives host performance.

Plants interact with a diversity of microorganisms that influence their growth and resilience, and they can therefore be considered as ecological entities, namely "plant holobionts," rather than as singular organisms. In a plant holobiont, the assembly of above- and belowground microbiota is ruled by host, microbial, and environmental factors. Upon microorganism perception, plants activate immune signaling resulting in the secretion of factors that modulate microbiota composition. Additionally, metabolic interdependencies and antagonism between microbes are driving forces for community assemblies. We argue that complex plant-microbe and intermicrobial interactions have been selected for during evolution and may promote the survival and fitness of plants and their associated microorganisms as holobionts. As part of this process, plants evolved metabolite-mediated strategies to selectively recruit beneficial microorganisms in their microbiota. Some of these microbiota members show host-adaptation, from which mutualism may rapidly arise. In the holobiont, microbiota members also co-evolved antagonistic activities that restrict proliferation of microbes with high pathogenic potential and can therefore prevent disease development. Co-evolution within holobionts thus ultimately drives plant performance.

Meet the Metaorganism: A web-based learning app for undergraduate and graduate biology students.

Meet the Metaorganism is a web-based learning app that combines three fundamental biological concepts (coevolution, community dynamics, and immune system) with latest scientific findings using the metaorganism as a central case study. In a transdisciplinary team of scientists, information designers, programmers, science communicators, and educators, we conceptualized and developed the app according to the latest didactic and scientific findings and aimed at setting new standards in visual design, digital knowledge transfer, and online education. A content management system allows continuous integration of new findings, which enables us to expand the app with the dynamics of the research field. Students can thus gain a close insight and connection to current research, and at the same time learn that knowledge is not static but grows dynamically. Especially in the realm of the easily accessible metaorganism research, visualization plays an essential role to keep complex processes understandable and memorable. Meet the Metaorganism is freely available online and can be accessed here: www.metaorganism.app.

Meta-organism gene expression reveals that the impact of nitrate enrichment on coral larvae is mediated by their associated Symbiodiniaceae and prokaryotic assemblages.

BACKGROUND: Coral meta-organisms consist of the coral, and its associated Symbiodiniaceae (dinoflagellate algae), bacteria, and other microbes. Corals can acquire photosynthates from Symbiodiniaceae, whilst Symbiodiniaceae uses metabolites from corals. Prokaryotic microbes provide Symbiodiniaceae with nutrients and support the resilience of corals as meta-organisms. Eutrophication is a major cause of coral reef degradation; however, its effects on the transcriptomic response of coral meta-organisms remain unclear, particularly for prokaryotic microbes associated with corals in the larval stage. To understand acclimation of the coral meta-organism to elevated nitrate conditions, we analyzed the physiological and transcriptomic responses of Pocillopora damicornis larvae, an ecologically important scleractinian coral, after 5 days of exposure to elevated nitrate levels (5, 10, 20, and 40 µM). RESULTS: The major differentially expressed transcripts in coral, Symbiodiniaceae, and prokaryotic microbes included those related to development, stress response, and transport. The development of Symbiodiniaceae was not affected in the 5 and 20 µM groups but was downregulated in the 10 and 40 µM groups. In contrast, prokaryotic microbe development was upregulated in the 10 and 40 µM groups and downregulated in the 5 and 20 µM groups. Meanwhile, coral larval development was less downregulated in the 10 and 40 µM groups than in the 5 and 20 µM groups. In addition, multiple larval, Symbiodiniaceae, and prokaryotic transcripts were significantly correlated with each other. The core transcripts in correlation networks were related to development, nutrient metabolism, and transport. A generalized linear mixed model, using least absolute shrinkage and selection operator, demonstrated that the Symbiodiniaceae could both benefit and cost coral larval development. Furthermore, the most significantly correlated prokaryotic transcripts maintained negative correlations with the physiological functions of Symbiodiniaceae. CONCLUSIONS: Results suggested that Symbiodiniaceae tended to retain more nutrients under elevated nitrate concentrations, thereby shifting the coral-algal association from mutualism towards parasitism. Prokaryotic microbes provided Symbiodiniaceae with essential nutrients and may control Symbiodiniaceae growth through competition, whereby prokaryotes can also restore coral larval development inhibited by Symbiodiniaceae overgrowth. Video Abstract.