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"Reitzel, Adam"
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Microbiota mediated plasticity promotes thermal adaptation in the sea anemone Nematostella vectensis
2022
At the current rate of climate change, it is unlikely that multicellular organisms will be able to adapt to changing environmental conditions through genetic recombination and natural selection alone. Thus, it is critical to understand alternative mechanisms that allow organisms to cope with rapid environmental changes. Here, we use the sea anemone
Nematostella vectensis
, which has evolved the capability of surviving in a wide range of temperatures and salinities, as a model to investigate the microbiota as a source of rapid adaptation. We long-term acclimate polyps of
Nematostella
to low, medium, and high temperatures, to test the impact of microbiota-mediated plasticity on animal acclimation. Using the same animal clonal line, propagated from a single polyp, allows us to eliminate the effects of the host genotype. The higher thermal tolerance of animals acclimated to high temperature can be transferred to non-acclimated animals through microbiota transplantation. The offspring fitness is highest from F0 females acclimated to high temperature and specific members of the acclimated microbiota are transmitted to the next generation. These results indicate that microbiota plasticity can contribute to animal thermal acclimation and its transmission to the next generation may represent a rapid mechanism for thermal adaptation.
This study shows that sea anemones acclimated to high temperatures exhibit increased resistance to thermal stress and that this improved fitness can be transferred by microbiome transplantation. These results indicate that plasticity mediated by the microbiota might be an important factor facilitating thermal adaptations in animals.
Journal Article
Genotype–environment interactions determine microbiota plasticity in the sea anemone Nematostella vectensis
by
Baldassarre, Laura
,
Reitzel, Adam M.
,
Fraune, Sebastian
in
Ambient temperature
,
Analysis
,
Animals
2023
Most multicellular organisms harbor microbial colonizers that provide various benefits to their hosts. Although these microbial communities may be host species- or even genotype-specific, the associated bacterial communities can respond plastically to environmental changes. In this study, we estimated the relative contribution of environment and host genotype to bacterial community composition in Nematostella vectensis , an estuarine cnidarian. We sampled N . vectensis polyps from 5 different populations along a north–south gradient on the Atlantic coast of the United States and Canada. In addition, we sampled 3 populations at 3 different times of the year. While half of the polyps were immediately analyzed for their bacterial composition by 16S rRNA gene sequencing, the remaining polyps were cultured under laboratory conditions for 1 month. Bacterial community comparison analyses revealed that laboratory maintenance reduced bacterial diversity by 4-fold, but maintained a population-specific bacterial colonization. Interestingly, the differences between bacterial communities correlated strongly with seasonal variations, especially with ambient water temperature. To decipher the contribution of both ambient temperature and host genotype to bacterial colonization, we generated 12 clonal lines from 6 different populations in order to maintain each genotype at 3 different temperatures for 3 months. The bacterial community composition of the same N . vectensis clone differed greatly between the 3 different temperatures, highlighting the contribution of ambient temperature to bacterial community composition. To a lesser extent, bacterial community composition varied between different genotypes under identical conditions, indicating the influence of host genotype. In addition, we identified a significant genotype x environment interaction determining microbiota plasticity in N . vectensis . From our results we can conclude that N . vectensis -associated bacterial communities respond plastically to changes in ambient temperature, with the association of different bacterial taxa depending in part on the host genotype. Future research will reveal how this genotype-specific microbiota plasticity affects the ability to cope with changing environmental conditions.
Journal Article
Micro and macroevolution of sea anemone venom phenotype
2023
Venom is a complex trait with substantial inter- and intraspecific variability resulting from strong selective pressures acting on the expression of many toxic proteins. However, understanding the processes underlying toxin expression dynamics that determine the venom phenotype remains unresolved. By interspecific comparisons we reveal that toxin expression in sea anemones evolves rapidly and that in each species different toxin family dictates the venom phenotype by massive gene duplication events. In-depth analysis of the sea anemone,
Nematostella vectensis
, revealed striking variation of the dominant toxin (
Nv1
) diploid copy number across populations (1-24 copies) resulting from independent expansion/contraction events, which generate distinct haplotypes.
Nv1
copy number correlates with expression at both the transcript and protein levels with one population having a near-complete loss of Nv1 production. Finally, we establish the dominant toxin hypothesis which incorporates observations in other venomous lineages that animals have convergently evolved a similar strategy in shaping their venom.
Venom is a complex trait with unresolved underlying toxin expression dynamics. Here, the authors compare expression across sea anemone species, revealing variation in dominant toxin diploid copy number across populations which generates distinct haplotypes.
Journal Article
Convergent shifts in host-associated microbial communities across environmentally elicited phenotypes
2018
Morphological plasticity is a genotype-by-environment interaction that enables organisms to increase fitness across varying environments. Symbioses with diverse microbiota may aid in acclimating to this variation, but whether the associated bacteria community is phenotype specific remains understudied. Here we induce morphological plasticity in three species of sea urchin larvae and measure changes in the associated bacterial community. While each host species has unique bacterial communities, the expression of plasticity results in the convergence on a phenotype-specific microbiome that is, in part, driven by differential association with α- and γ-proteobacteria. Furthermore, these results suggest that phenotype-specific signatures are the product of the environment and are correlated with ingestive and digestive structures. By manipulating diet quantity over time, we also show that differentially associating with microbiota along a phenotypic continuum is bidirectional. Taken together, our data support the idea of a phenotype-specific microbial community and that phenotypic plasticity extends beyond a genotype-by-environment interaction.
Symbiotic microbial communities aid their hosts through developmental and environmental transitions. Here, the authors show that host morphological plasticity is associated with predictable changes in a phenotype-specific microbiome in three species of sea urchin larvae.
Journal Article
Decoupling behavioral and transcriptional responses to color in an eyeless cnidarian
by
Reitzel, Adam M.
,
Leach, Whitney B.
in
Analysis
,
Animal behavior
,
Animal Genetics and Genomics
2020
Background
Animals have specific molecular, physiological, and behavioral responses to light that are influenced by wavelength and intensity. Predictable environmental changes – predominantly solar and lunar cycles – drive endogenous daily oscillations by setting internal pacemakers, otherwise known as the circadian clock. Cnidarians have been a focal group to discern the evolution of light responsiveness due to their phylogenetic position as a sister phylum to bilaterians and broad range of light-responsive behaviors and physiology. Marine species that occupy a range of depths will experience different ranges of wavelengths and light intensities, which may result in variable phenotypic responses. Here, we utilize the eyeless sea anemone
Nematostella vectensis
, an estuarine anemone that typically resides in shallow water habitats, to compare behavioral and molecular responses when exposed to different light conditions.
Results
Quantitative measures of locomotion clearly showed that this species responds to light in the blue and green spectral range with a circadian activity profile, in contrast to a circatidal activity profile in the red spectral range and in constant darkness. Differences in average day/night locomotion was significant in each condition, with overall peak activity during the dark period. Comparative analyses of 96 transcriptomes from individuals sampled every 4 h in each lighting treatment revealed complex differences in gene expression between colors, including in many of the genes likely involved in the cnidarian circadian clock. Transcriptional profiling showed the majority of genes are differentially expressed when comparing mid-day with mid-night, and mostly in red light. Gene expression profiles were largely unique in each color, although animals in blue and green were overall more similar to each other than to red light.
Conclusions
Together, these analyses support the hypothesis that cnidarians are sensitive to red light, and this perception results in a rich transcriptional and divergent behavioral response. Future work determining the specific molecular mechanisms driving the circadian and potential circatidal rhythms measured here would be impactful to connect gene expression variation with behavioral variation in this eyeless species.
Journal Article
Bacterial community dynamics during embryonic and larval development of three confamilial echinoids
2019
Development of some animals is influenced by and, in some cases, dependent on the associated microbiota. The timing of when associated bacterial communities are established during the development of marine invertebrates and their subsequent dynamics across stages are known for only a few species. Here, we compared the bacterial communities of 3 confamilial echinoids from egg to juvenile using sequence-based approaches. Bacterial communities are established on unfertilized eggs and change gradually during embryonic and larval development. Despite the differences amongst these pre-metamorphic stages, approximately 30% of operational taxonomic units (OTUs) identified in association with unfertilized eggs were present in the juveniles. During embryonic development, host-associated communities diverged from the environmental microbiota but later converged following the onset of larval feeding. Taken together, the data presented here support the hypothesis that bacterial communities are established prior to fertilization and community composition shifts gradually thereafter, all the while remaining distinct from the environment. Future work will need to determine the relative influence of the host and bacteria–bacteria interactions in shaping the associated bacterial community to more broadly determine the potential functional importance of bacteria during the development of larval sea urchins and benthic marine invertebrates.
Journal Article
Light Entrained Rhythmic Gene Expression in the Sea Anemone Nematostella vectensis: The Evolution of the Animal Circadian Clock
by
Behrendt, Lars
,
Reitzel, Adam M.
,
Tarrant, Ann M.
in
Acropora millepora
,
Analysis
,
Animal behavior
2010
Circadian rhythms in behavior and physiology are the observable phenotypes from cycles in expression of, interactions between, and degradation of the underlying molecular components. In bilaterian animals, the core molecular components include Timeless-Timeout, photoreceptive cryptochromes, and several members of the basic-loop-helix-Per-ARNT-Sim (bHLH-PAS) family. While many of core circadian genes are conserved throughout the Bilateria, their specific roles vary among species. Here, we identify and experimentally study the rhythmic gene expression of conserved circadian clock members in a sea anemone in order to characterize this gene network in a member of the phylum Cnidaria and to infer critical components of the clockwork used in the last common ancestor of cnidarians and bilaterians.
We identified homologs of circadian regulatory genes in the sea anemone Nematostella vectensis, including a gene most similar to Timeout, three cryptochromes, and several key bHLH-PAS transcription factors. We then maintained N. vectensis either in complete darkness or in a 12 hour light: 12 hour dark cycle in three different light treatments (blue only, full spectrum, blue-depleted). Gene expression varied in response to light cycle and light treatment, with a particularly strong pattern observed for NvClock. The cryptochromes more closely related to the light-sensitive clade of cryptochromes were upregulated in light treatments that included blue wavelengths. With co-immunoprecipitation, we determined that heterodimerization between CLOCK and CYCLE is conserved within N. vectensis. Additionally, we identified E-box motifs, DNA sequences recognized by the CLOCK:CYCLE heterodimer, upstream of genes showing rhythmic expression.
This study reveals conserved molecular and functional components of the circadian clock that were in place at the divergence of the Cnidaria and Bilateria, suggesting the animal circadian clockwork is more ancient than previous data suggest. Characterizing circadian regulation in a cnidarian provides insight into the early origins of animal circadian rhythms and molecular regulation of environmentally cued behaviors.
Journal Article
Dynamics of venom composition across a complex life cycle
by
Sunagar, Kartik
,
Sachkova, Maria Y
,
Columbus-Shenkar, Yaara Y
in
Animals
,
Aquatic ecosystems
,
Biochemistry
2018
Little is known about venom in young developmental stages of animals. The appearance of toxins and stinging cells during early embryonic stages in the sea anemone Nematostella vectensis suggests that venom is already expressed in eggs and larvae of this species. Here, we harness transcriptomic, biochemical and transgenic tools to study venom production dynamics in Nematostella. We find that venom composition and arsenal of toxin-producing cells change dramatically between developmental stages of this species. These findings can be explained by the vastly different interspecific interactions of each life stage, as individuals develop from a miniature non-feeding mobile planula to a larger sessile polyp that predates on other animals and interact differently with predators. Indeed, behavioral assays involving prey, predators and Nematostella are consistent with this hypothesis. Further, the results of this work suggest a much wider and dynamic venom landscape than initially appreciated in animals with a complex life cycle. Some animals produce a mixture of toxins, commonly known as venom, to protect themselves from predators and catch prey. Cnidarians – a group of animals that includes sea anemones, jellyfish and corals – have stinging cells on their tentacles that inject venom into the animals they touch. The sea anemone Nematostella goes through a complex life cycle. Nematostella start out life in eggs. They then become swimming larvae, barely visible to the naked eye, that do not feed. Adult Nematostella are cylindrical, stationary ‘polyps’ that are several inches long. They use tentacles at the end of their tube-like bodies to capture small aquatic animals. Sea anemones therefore change how they interact with predators and prey at different stages of their life. Most research on venomous animals focuses on adults, so until now it was not clear whether the venom changes along their maturation. Columbus-Shenkar, Sachkova et al. genetically modified Nematostella so that the cells that produce distinct venom components were labeled with different fluorescent markers. The composition of the venom could then be linked to how the anemones interacted with their fish and shrimp predators at each life stage. The results of the experiments showed that Nematostella mothers pass on a toxin to their eggs that makes them unpalatable to predators. Larvae then produce high levels of other toxins that allow them to incapacitate or kill potential predators. Adults have a different mix of toxins that likely help them capture prey. Venom is often studied because the compounds it contains have the potential to be developed into new drugs. The jellyfish and coral relatives of Nematostella may also produce different venoms at different life stages. This means that there are likely to be many toxins that we have not yet identified in these animals. As some jellyfish venoms are very active on humans and reef corals have a pivotal role in ocean ecology, further research into the venoms produced at different life stages could help us to understand and preserve marine ecosystems, as well as having medical benefits.
Journal Article
Influence of Temperature and Saline Conditions on Bacteria Naturally Associated With the Cnidarian Host Nematostella vectensis
2025
The associated microorganisms (“microbiome”) of multicellular individuals (“host”) are important for the physiology and survival of the host. Individual bacterial species vary in environmental tolerances that may limit their associations with hosts, especially when their range of survivable conditions is narrower. To elucidate the roles for different environmental niche spaces of bacteria that may compose the microbiome, we evaluated the survival and growth of individual and combinations of bacteria with and without an animal host, the sea anemone Nematostella vectensis (Cnidaria, Anthozoa). We assessed 62 environmental bacteria from seven genera ( Alteromonas , Bacillus , Grimontia , Photobacterium , Pseudoalteromonas , Shewanella , and Vibrio ) isolated from six estuaries and the host to determine their tolerance across a gradient of temperatures (30°–40°C) and salinities (5–30 ppt). Growth rates and plate counts revealed members of the Vibrio genus had the highest growth rate at higher salinities (15 and 30 ppt), while Bacillus and Alteromonas spp. exhibited consistent growth over a broader range of salinities and temperatures. Only 15% of isolates were capable of growth at the combination of highest temperature and lowest salinity (40°C, 5 ppt), suggesting that these environmentally relevant conditions may limit microbiome diversity. We further assessed three isolates ( Bacillus velezensis , Pseudoalteromonas spiralis , and Vibrio diabolicus ) for how bacterial growth changed when associated with N. vectensis . When anemones were exposed to environmentally relevant heat stress over 3 days, bacterial concentrations varied significantly. P. spiralis grew more under lower salinities and maintained stable concentrations. Conversely, V. diabolicus grew more with higher salinity and maintained these high concentrations in nearly all conditions. At sustained extreme temperatures for the anemones, the microbial composition exerted a small impact on survival. Together, these results support that environmental conditions are important drivers for the relative abundance of particular bacteria in the context of the host′s microbiome.
Journal Article
Transcriptomic Analysis of Four Cerianthid (Cnidaria, Ceriantharia) Venoms
2020
Tube anemones, or cerianthids, are a phylogenetically informative group of cnidarians with complex life histories, including a pelagic larval stage and tube-dwelling adult stage, both known to utilize venom in stinging-cell rich tentacles. Cnidarians are an entirely venomous group that utilize their proteinaceous-dominated toxins to capture prey and defend against predators, in addition to several other ecological functions, including intraspecific interactions. At present there are no studies describing the venom for any species within cerianthids. Given their unique development, ecology, and distinct phylogenetic-placement within Cnidaria, our objective is to evaluate the venom-like gene diversity of four species of cerianthids from newly collected transcriptomic data. We identified 525 venom-like genes between all four species. The venom-gene profile for each species was dominated by enzymatic protein and peptide families, which is consistent with previous findings in other cnidarian venoms. However, we found few toxins that are typical of sea anemones and corals, and furthermore, three of the four species express toxin-like genes closely related to potent pore-forming toxins in box jellyfish. Our study is the first to provide a survey of the putative venom composition of cerianthids and contributes to our general understanding of the diversity of cnidarian toxins.
Journal Article