scholarly journals Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome

2020 ◽  
Vol 16 (2) ◽  
pp. 20190738
Author(s):  
Benjamin M. Titus ◽  
Robert Laroche ◽  
Estefanía Rodríguez ◽  
Herman Wirshing ◽  
Christopher P. Meyer

All eukaryotic life engages in symbioses with a diverse community of bacteria that are essential for performing basic life functions. In many cases, eukaryotic organisms form additional symbioses with other macroscopic eukaryotes. The tightly linked physical interactions that characterize many macroscopic symbioses create opportunities for microbial transfer, which likely affects the diversity and function of individual microbiomes, and may ultimately lead to microbiome convergence between distantly related taxa. Here, we sequence the microbiomes of five species of clownfish-hosting sea anemones that co-occur on coral reefs in the Maldives. We test the importance of evolutionary history, clownfish symbiont association, and habitat on the taxonomic and predicted functional diversity of the microbiome, and explore signals of microbiome convergence in anemone taxa that have evolved symbioses with clownfishes independently. Our data indicate that host identity and clownfish association shapes the majority of the taxonomic diversity of the clownfish-hosting sea anemone microbiome, and predicted functional microbial diversity analyses demonstrate a convergence among host anemone microbiomes, which reflect increased functional diversity over individuals that do not host clownfishes. Further, we identify upregulated predicted microbial functions that are likely affected by clownfish presence. Taken together our study potentially reveals an even deeper metabolic coupling between clownfishes and their host anemones, and what could be a previously unknown mutualistic benefit to anemones that are symbiotic with clownfishes.

2019 ◽  
Author(s):  
Benjamin M. Titus ◽  
Robert Laroche ◽  
Estefanía Rodríguez ◽  
Herman Wirshing ◽  
Christopher P. Meyer

AbstractAll eukaryotic life engages in symbioses with a diverse community of bacteria that are essential for performing basic life functions. In many cases, eukaryotic organisms form additional symbioses with other macroscopic eukaryotes. The tightly-linked physical interactions that characterize many macroscopic symbioses creates opportunities for microbial transfer, which likely affects the diversity and function of individual microbiomes, and may ultimately lead to microbiome convergence between distantly related taxa. Here, we sequence the microbiomes of five species of clownfish-hosting sea anemones that co-occur on coral reefs in the Maldives. We test the importance of evolutionary history, clownfish symbiont association, and habitat on the genetic and predicted functional diversity of the microbiome, and explore signals of microbiome convergence in anemone taxa that have evolved symbioses with clownfishes independently. Our data indicate that host identity shapes the majority of the genetic diversity of the clownfish-hosting sea anemone microbiome, but predicted functional microbial diversity analyses demonstrate a convergence among host anemone microbiomes, which reflect increased functional diversity over individuals that do not host clownfishes. Further, we identify up-regulated microbial functions in host anemones that are likely affected by clownfish presence. Taken together our study reveals an even deeper metabolic coupling between clownfishes and their host anemones, and what could be a previously unknown mutualistic benefit to anemones that are symbiotic with clownfishes.


2017 ◽  
Author(s):  
Arnaud Meng ◽  
Camille Marchet ◽  
Erwan Corre ◽  
Pierre Peterlongo ◽  
Adriana Alberti ◽  
...  

AbstractBackgroundStudy of meta-transcriptomic datasets involving non-model organisms represents bioinformatic challenges. The production of chimeric sequences and our inability to distinguish the taxonomic origins of the sequences produced are inherent and recurrent difficulties in de novo assembly analyses. The study of holobiont transcriptomes shares similarities with meta-transcriptomic, and hence, is also affected by challenges invoked above. Here we propose an innovative approach to tackle such difficulties which was applied to the study of marine holobiont models as a proof of concept.ResultsWe considered three holobionts models, of which two transcriptomes were previously assembled and published, and a yet unpublished transcriptome, to analyze their raw reads and assign them to the host and/or to the symbiont(s) using Short Read Connector, a k-mer based similarity method. We were able to define four distinct categories of reads for each holobiont transcriptome: host reads, symbiont reads, shared reads and unassigned reads. The result of the independent assemblies for each category within a transcriptome led to a significant diminution of de novo assembled chimeras compared to classical assembly methods. Combining independent functional and taxonomic annotations of each partner’s transcriptome is particularly convenient to explore the functional diversity of an holobiont. Finally, our strategy allowed to propose new functional annotations for two well-studied holobionts and a first transcriptome from a planktonic Radiolaria-Dinophyta system forming widespread symbiotic association for which our knowledge is limited. ConclusionsIn contrast to classical assembly approaches, our bioinformatic strategy not only allows biologists to studying separately host and symbiont data from a holobiont mixture, but also generates improved transcriptome assemblies. The use of Short Read Connector has proven to be an effective way to tackle meta-transcriptomic challenges to study holobiont systems composed of either well-studied or poorly characterized symbiotic lineages such as the newly sequenced marine plankton Radiolaria-Dinophyta symbiosis and ultimately expand our knowledge about these marine symbiotic associations.


2020 ◽  
Vol 287 (1940) ◽  
pp. 20201860
Author(s):  
Samuel A. Bedgood ◽  
Sarah E. Mastroni ◽  
Matthew E. S. Bracken

Mutualistic symbioses are common, especially in nutrient-poor environments where an association between hosts and symbionts can allow the symbiotic partners to persist and collectively out-compete non-symbiotic species. Usually these mutualisms are built on an intimate transfer of energy and nutrients (e.g. carbon and nitrogen) between host and symbiont. However, resource availability is not consistent, and the benefit of the symbiotic association can depend on the availability of resources to mutualists. We manipulated the diets of two temperate sea anemone species in the genus Anthopleura in the field and recorded the responses of sea anemones and algal symbionts in the family Symbiodiniaceae to our treatments. Algal symbiont density, symbiont volume and photosynthetic efficiency of symbionts responded to changes in sea anemone diet, but the responses depended on the species of sea anemone. We suggest that temperate sea anemones and their symbionts can respond to changes in anemone diet, modifying the balance between heterotrophy and autotrophy in the symbiosis. Our data support the hypothesis that symbionts are upregulated or downregulated based on food availability, allowing for a flexible nutritional strategy based on external resources.


2016 ◽  
Author(s):  
Doriane Stagnol ◽  
Lise Bacouillard ◽  
Dominique Davoult

Among the potential indicators of biodiversity, those based on the functional traits of species are interesting because they measure the aspects of diversity that potentially affect community assembly and function. However, trait-based approaches are still rarely considered and little is known about the degree to which taxonomic diversity (TD) and functional diversity (FD) are correlated. Yet, this relationship is thought to depend on the extent of ecological redundancy within the assemblage, i.e. the number of taxonomically distinct species that exhibit similar ecological functions. In this study, we characterized taxonomic and functional diversity within and between two marine habitats (rocky shore vs mudflats) under human-induced disturbances. Models were also used to test whether the relationship between TD and FD differed according to the indices used to characterize them. We found little effect of human disturbance on the shape of the TD-FD relationship, whereas communities of the mudflat appeared to be less redundant than those of rocky shore. This could be explained by the assembly rules of ecosystems: biotic filtering (competition and resource partitioning) reduces redundancy by selecting for functionally dissimilar species, whereas abiotic filtering increases redundancy by selecting for similar species sharing adaptations to a particular environment. The rocky shore environment is characterized by heterogeneity that allows the formation of distinct ecological niches that can be colonized by similar species: the abiotic filtering does not limit the redundancy permitted by habitat. Conversely, in the more homogeneous environment of mudflat, the biotic filter mitigates redundancy. Trait-mediated abiotic filtering appears to play an important role in community assembly in complex habitats, whereas the relative importance of competitive exclusion appears to be greater in homogeneous habitats.


Author(s):  
Doriane Stagnol ◽  
Lise Bacouillard ◽  
Dominique Davoult

Among the potential indicators of biodiversity, those based on the functional traits of species are interesting because they measure the aspects of diversity that potentially affect community assembly and function. However, trait-based approaches are still rarely considered and little is known about the degree to which taxonomic diversity (TD) and functional diversity (FD) are correlated. Yet, this relationship is thought to depend on the extent of ecological redundancy within the assemblage, i.e. the number of taxonomically distinct species that exhibit similar ecological functions. In this study, we characterized taxonomic and functional diversity within and between two marine habitats (rocky shore vs mudflats) under human-induced disturbances. Models were also used to test whether the relationship between TD and FD differed according to the indices used to characterize them. We found little effect of human disturbance on the shape of the TD-FD relationship, whereas communities of the mudflat appeared to be less redundant than those of rocky shore. This could be explained by the assembly rules of ecosystems: biotic filtering (competition and resource partitioning) reduces redundancy by selecting for functionally dissimilar species, whereas abiotic filtering increases redundancy by selecting for similar species sharing adaptations to a particular environment. The rocky shore environment is characterized by heterogeneity that allows the formation of distinct ecological niches that can be colonized by similar species: the abiotic filtering does not limit the redundancy permitted by habitat. Conversely, in the more homogeneous environment of mudflat, the biotic filter mitigates redundancy. Trait-mediated abiotic filtering appears to play an important role in community assembly in complex habitats, whereas the relative importance of competitive exclusion appears to be greater in homogeneous habitats.


2021 ◽  
Author(s):  
Leslie S Babonis ◽  
Camille Enjolras ◽  
Abigail J Reft ◽  
Brent M Foster ◽  
Fredrik Hugosson ◽  
...  

Cnidocytes are the explosive stinging cells found only in cnidarians (corals, jellyfish, etc). Specialized for prey capture and defense, cnidocytes are morphologically complex and vary widely in form and function across taxa; how such diversity evolved is unknown. Using CRISPR/Cas9-mediated genome editing in the burrowing sea anemone Nematostella vectensis, we show that a single transcription factor (NvSox2) acts as a binary switch between two alternative cnidocyte fates. Knockout of NvSox2 caused a complete transformation of nematocytes (piercing cells) into spirocytes (ensnaring cells). The type of spirocyte induced by NvSox2 knockout (robust spirocyte) is not normally found in N. vectensis but is common in sea anemones from other habitats. Homeotic control of cell fate provides a mechanistic explanation for the discontinuous distribution of cnidocyte types across cnidarians and demonstrates how simple counts of cell types can underestimate biodiversity.


Genetics ◽  
1998 ◽  
Vol 150 (2) ◽  
pp. 553-562
Author(s):  
Margaret I Kanipes ◽  
John E Hill ◽  
Susan A Henry

Abstract The isolation of mutants of Schizosaccharomyces pombe defective in the synthesis of phosphatidylcholine via the methylation of phosphatidylethanolamine is reported. These mutants are choline auxotrophs and fall into two unlinked complementation groups, cho1 and cho2. We also report the analysis of the cho1+ gene, the first structural gene encoding a phospholipid biosynthetic enzyme from S. pombe to be cloned and characterized. The cho1+ gene disruption mutant (cho1Δ) is viable if choline is supplied and resembles the cho1 mutants isolated after mutagenesis. Sequence analysis of the cho1+ gene indicates that it encodes a protein closely related to phospholipid methyltransferases from Saccharomyces cerevisiae and rat. Phospholipid methyltransferases encoded by a rat liver cDNA and the S. cerevisiae OPI3 gene are both able to complement the choline auxotrophy of the S. pombe cho1 mutants. These results suggest that both the structure and function of the phospholipid N-methyltransferases are broadly conserved among eukaryotic organisms.


Author(s):  
Michel Praet-Van

This ultrastructural investigation of gametogenesis in a deep-sea anemone of the Bay of Biscay trawled around 2000 m depth, contributes to the knowledge of biology and strategy of reproduction of deep-sea benthos.This sea anemone is dioecious. The sperm appears very similar to those of shallow water sea anemones of the genus, Calliactis. The ultrastructural investigation of oogenesis allows the characteristics of the stages of previtellogenesis and vitellogenesis to be defined. The latter begins with a period of lipogenesis correlated with the formation of a trophonema. Mature oocytes measure up to 180 (im in diameter. Study of spermatogenesis and oogenesis reveals that spawning occurs in April/May. In males, the main area of testicular cysts, full of sperm, reaches maximal development from March to May and, in females, the percentage of mature oocytes decreases from 33% in April to 1% in May.Spawning may be induced by the advent in the deep-sea of the products of the spring phytoplankton bloom. This period of spawning, during the increased deposition of organic matter to the deep-sea floor, may be an advantageous strategy for early development of Paracalliactis.


1971 ◽  
Vol 55 (3) ◽  
pp. 611-640
Author(s):  
ELAINE A. ROBSON

1. In Gonactinia well-developed ectodermal muscle and nerve-net extend over the column and crown and play an important part in the anemone's behaviour. 2. Common sequences of behaviour are described. Feeding is a series of reflex contractions of different muscles by means of which plankton is caught and swallowed. Walking, in the form of brief looping steps, differs markedly in that it continues after interruptions. Anemones also swim with rapid tentacle strokes after contact with certain nudibranch molluscs, strong mechanical disturbance or electrical stimulation. 3. Swimming is attributed to temporary excitation of a diffuse ectodermal pacemaker possibly situated in the upper column. 4. From the results of electrical and mechanical stimulation it is concluded that the endodermal neuromuscular system resembles that of other anemones but that the properties of the ectodermal neuromuscular system require a new explanation. The size and spread of responses to electric shocks vary with intensity, latency is variable and there is a tendency to after-discharge. There is precise radial localization, for example touching a tentacle or the column causes it to bend towards or away from the stimulus. 5. A model to explain these and other features includes multipolar nerve cells closely linked to the nerve-net which would act as intermediate motor units, causing local contraction of the ectodermal muscle. This scheme can be applied to other swimming anemones but there is no evidence that it holds for sea anemones generally.


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