Emerging Sponge Models of Animal-Microbe Symbioses

Sponges have a significant impact on marine benthic communities, they are of biotechnological interest owing to their production of bioactive natural compounds, and they promise to provide insights into conserved mechanisms of host–microbe interactions in basal metazoans. The natural variability of sponge-microbe associations across species and environments provides a meaningful ecological and evolutionary framework to investigate animal-microbial symbiosis through experimentation in the field and also in aquaria. In addition, next-generation sequencing technologies have shed light on the genomic repertoire of the sponge host and revealed metabolic capacities and symbiotic lifestyle features of their microbiota. However, our understanding of symbiotic mechanisms is still in its infancy. Here, we discuss the potential and limitations of the sponge-microbe symbiosis as emerging models for animal-associated microbiota

Bdellovibrio and Like Organisms Are Predictors of Microbiome Diversity in Distinct Host Groups

Biodiversity is generally believed to be a main determinant of ecosystem functioning. This principle also applies to the microbiome and could consequently contribute to host health. According to ecological theory, communities are shaped by top predators whose direct and indirect interactions with community members cause stability and diversity. Bdellovibrio and like organisms (BALOs) are a neglected group of predatory bacteria that feed on Gram-negative bacteria and can thereby influence microbiome composition. We asked whether BALOs can predict biodiversity levels in microbiomes from distinct host groups and environments. We demonstrate that genetic signatures of BALOs are commonly found within the 16S rRNA reads from diverse host taxa. In many cases, their presence, abundance, and especially richness are positively correlated with overall microbiome diversity. Our findings suggest that BALOs can act as drivers of microbial alpha-diversity and should therefore be considered candidates for the restoration of microbiomes and the prevention of dysbiosis

Function and Evolution of Nuclear Receptors in Environmental-Dependent Postembryonic Development

Nuclear receptors (NRs) fulfill key roles in the coordination of postembryonal developmental transitions in animal species. They control the metamorphosis and sexual maturation in virtually all animals and by that the two main environmental-dependent developmental decision points. Sexual maturation and metamorphosis are controlled by steroid receptors and thyroid receptors, respectively in vertebrates, while both processes are orchestrated by the ecdysone receptor (EcR) in insects. The regulation of these processes depends on environmental factors like nutrition, temperature, or photoperiods and by that NRs form evolutionary conserved mediators of phenotypic plasticity. While the mechanism of action for metamorphosis and sexual maturation are well studied in model organisms, the evolution of these systems is not entirely understood and requires further investigation. We here review the current knowledge of NR involvement in metamorphosis and sexual maturation across the animal tree of life with special attention to environmental integration and evolution of the signaling mechanism. Furthermore, we compare commonalities and differences of the different signaling systems. Finally, we identify key gaps in our knowledge of NR evolution, which, if sufficiently investigated, would lead to an importantly improved understanding of the evolution of complex signaling systems, the evolution of life history decision points, and, ultimately, speciation events in the metazoan kingdom

Carrying Capacity and Colonization Dynamics of Curvibacter in the Hydra Host Habitat

Most eukaryotic species are colonized by a microbial community – the microbiota – that is acquired during early life stages and is critical to host development and health. Much research has focused on the microbiota biodiversity during the host life, however, empirical data on the basic ecological principles that govern microbiota assembly is lacking. Here we quantify the contribution of colonizer order, arrival time and colonization history to microbiota assembly on a host. We established the freshwater polyp Hydra vulgaris and its dominant colonizer Curvibacter as a model system that enables the visualization and quantification of colonizer population size at the single cell resolution, in vivo, in real time. We estimate the carrying capacity of a single Hydra polyp as 2 × 105 Curvibacter cells, which is robust among individuals and time. Colonization experiments reveal a clear priority effect of first colonizers that depends on arrival time and colonization history. First arriving colonizers achieve a numerical advantage over secondary colonizers within a short time lag of 24 h. Furthermore, colonizers primed for the Hydra habitat achieve a numerical advantage in the absence of a time lag. These results follow the theoretical expectations for any bacterial habitat with a finite carrying capacity. Thus, Hydra colonization and succession processes are largely determined by the habitat occupancy over time and Curvibacter colonization history. Our experiments provide empirical data on the basic steps of host-associated microbiota establishment – the colonization stage. The presented approach supplies a framework for studying habitat characteristics and colonization dynamics within the host–microbe setting

The Role of DNA Methylation in Genome Defense in Cnidaria and Other Invertebrates

Considerable attention has recently been focused on the potential involvement of DNA methylation in regulating gene expression in cnidarians. Much of this work has been centered on corals, in the context of changes in methylation perhaps facilitating adaptation to higher seawater temperatures and other stressful conditions. Although first proposed more than 30 years ago, the possibility that DNA methylation systems function in protecting animal genomes against the harmful effects of transposon activity has largely been ignored since that time. Here, we show that transposons are specifically targeted by the DNA methylation system in cnidarians, and that the youngest transposons (i.e., those most likely to be active) are most highly methylated. Transposons in longer and highly active genes were preferentially methylated and, as transposons aged, methylation levels declined, reducing the potentially harmful side effects of CpG methylation. In Cnidaria and a range of other invertebrates, correlation between the overall extent of methylation and transposon content was strongly supported. Present transposon burden is the dominant factor in determining overall level of genomic methylation in a range of animals that diverged in or before the early Cambrian, suggesting that genome defense represents the ancestral role of CpG methylation

Predicted bacterial interactions affect in vivo microbial colonization dynamics in Nematostella

The maintenance and resilience of host-associated microbiota during development is a fundamental process influencing the fitness of many organisms. Several host properties were identified as influencing factors on bacterial colonization, including the innate immune system, mucus composition and diet. In contrast, the importance of bacteria-bacteria interactions on host colonization is less understood. Here, we use bacterial abundance data of the marine model organism Nematostella vectensis to reconstruct potential bacteria-bacteria interactions through co-occurrence networks. The analysis indicates that bacteria-bacteria interactions are dynamic during host colonization and change according to the host’s developmental stage. To assess the predictive power of inferred interactions, we tested bacterial isolates with predicted cooperative or competitive behavior for their ability to influence bacterial recolonization dynamics. Within three days of recolonization all tested bacterial isolates affected bacterial community structure, while only competitive bacteria increased bacterial diversity. Already one week after recolonization almost no differences in bacterial community structure could be observed between control and treatments. These results show that predicted competitive bacteria can influence community structure for a short period of time, verifying the in silico predictions. However, within one week, the effects of the bacterial isolates are neutralized, indicating a high degree of resilience of the bacterial community. Hanna Domin1, Yazmín H. Zurita-Gutiérrez2, Marco Scotti3, Jann Buttlar1, Ute Hentschel Humeida2 and Sebastian Fraune1

Environmental bacteria increase population growth of hydra at low temperature

Multicellular organisms engage in complex ecological interactions with microorganisms, some of which are harmful to the host’s health and fitness (e.g., pathogens or toxin-producing environmental microbiota), while others are either beneficial or have a neutral impact (as seen in components of host-associated microbiota). Although environmental microorganisms are generally considered to have no significant impact on animal fitness, there is evidence suggesting that exposure to these microbes might be required for proper immune maturation and research in vertebrates has shown that developing in a sterile environment detrimentally impacts health later in life. However, it remains uncertain whether such beneficial effects of environmental microorganisms are present in invertebrates that lack an adaptive immune system. In the present study, we conducted an experiment with field-collected Hydra oligactis, a cold-adapted freshwater cnidarian. We cultured these organisms in normal and autoclaved lake water at two distinct temperatures: 8°C and 12°C. Our findings indicated that polyps maintained in sterilized lake water displayed reduced population growth that depended on temperature, such that the effect was only present on 8°C. To better understand the dynamics of microbial communities both inhabiting polyps and their surrounding environment we conducted 16S sequencing before and after treatment, analyzing samples from both the polyps and the water. As a result of culturing in autoclaved lake water, the polyps showed a slightly altered microbiota composition, with some microbial lineages showing significant reduction in abundance, while only a few displayed increased abundances. The autoclaved lake water was recolonized, likely from the surface of hydra polyps, by a complex albeit different community of bacteria, some of which (such as Pseudomonas, Flavobacteriaceae) might be pathogenic to hydra. The abundance of the intracellular symbiont Polynucleobacter was positively related to hydra population size. These findings indicate that at low temperature environmental microbiota can enhance population growth rate in hydra, suggesting that environmental microorganisms can provide benefits to animals even in the absence of an adaptive immune system

Traffic-related pollution (NO2 and CO) and its association with asthma symptoms among 10-11 year old children in Malaysia

Introduction: Children attending schools located close to major traffic sources are exposed to higher indoor air pollution levels due to infiltration of outdoor air pollutants. This study investigates the respiratory health of Malaysian schoolchildren in relation to indoor air pollution in schools and at home. Methods: This cross-sectional study was conducted among 2,164 schoolchildren aged 10-11 years in 35 urban and semi-rural schools in Kuala Lumpur Negeri Sembilan. Parents completed the International Study of Asthma and Allergy in Childhood questionnaire and provided information on the home environment and socio demographic background. Concentrations of NO2 and CO were measured indoors and outdoors of 14 schools. Results: The mean (standard deviation (SD)) indoor exposure to concentrations of air pollutants measured in Malaysian schools were: 42.9 (8.77) μg/m3 of NO2 and 3.16 (2.47) ppm of CO in urban schools and 12.4 (8.79) μg/m3 of NO2 and 0.33 (0.18) ppm of CO respectively for semi-rural schools. The prevalence of asthma was significantly higher among urban compared to semi-rural children. Ever wheeze was more common in urban areas (14.3%) compared to semi-rural areas (10.6%) as was current wheeze (urban 9.1%; semi-rural 6.2%), nocturnal cough (urban 12.0%; semi-rural 7.2%) and most other symptoms. The 3 main predictors of nocturnal cough were the presence of a current smoker at home (OR 1.97; 95% CI: 1.31-2.96), the absence of exhaust system in the kitchen (OR 1.67; 95% CI: 1.03-2.68) and the use of air conditioning (OR 3.10; 95% CI: 1.37-5.71). Self-reported asthma was predicted by the occupation of mothers; managerial positions (OR 1.78; 95% CI: 1.21-2.62), mothers working in the armed forces (OR 1.92; 95% CI: 1.32- 2.78) and fathers with a high school level of education (OR 0.46; 95% CI: 0.26- 0.82) while exposure to SHS of ≥4 hours per day (OR 2.53; 95% CI: 1.55-4.14) explained approximately 6.0% of the likelihood of reporting doctor-diagnosed asthma. Conclusion: This study has identified that many Malaysian schoolchildren experience exposure to air pollution indoors that exceeds WHO guidance limits for NO2 pollution but did not exceed the RMAQG levels. Considering that traffic-related sources largely contribute towards NO2 concentrations, compliance with the standards is not indicative of the reduced health risks for air pollution exposures

Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches

Current research highlights the importance of associated microbes in contributing to the functioning, health, and even adaptation of their animal, plant, and fungal hosts. As such, we are witnessing a shift in research that moves away from focusing on the eukaryotic host sensu stricto to research into the complex conglomerate of the host and its associated microorganisms (i.e., microbial eukaryotes, archaea, bacteria, and viruses), the so-called metaorganism, as the biological entity. While recent research supports and encourages the adoption of such an integrative view, it must be understood that microorganisms are not involved in all host processes and not all associated microorganisms are functionally important. As such, our intention here is to provide a critical review and evaluation of perspectives and limitations relevant to studying organisms in a metaorganism framework and the functional toolbox available to do so. We note that marker gene-guided approaches that primarily characterize microbial diversity are a first step in delineating associated microbes but are not sufficient to establish proof of their functional relevance. More sophisticated tools and experiments are necessary to reveal the specific functions of associated microbes. This can be accomplished through the study of metaorganisms in less complex environments, the targeted manipulation of microbial associates, or work at the mechanistic level with the toolbox available in model systems. We conclude that the metaorganism framework is a powerful new concept to help provide answers to longstanding biological questions such as the evolution and ecology of organismal complexity and the importance of organismal symbioses to ecosystem functioning. The intricacy of the metaorganism requires a holistic framework combining reductionist and integrative approaches to resolve metaorganism identities and to disclose the various roles that microorganisms play in the biology of their hosts