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Diet-Dependent Gene Expression Highlights the Importance Of www.nature.com/scientificreports OPEN Diet-dependent gene expression highlights the importance of Cytochrome P450 in detoxifcation Received: 27 April 2018 Accepted: 15 October 2018 of algal secondary metabolites in a Published: xx xx xxxx marine isopod Pierre De Wit 1, Keith Yamada 2, Marina Panova1, Carl André1 & Kerstin Johannesson1 Isopods of the genus Idotea have an unusual ability to feed on algae containing high amounts of chemical defense molecules, such as species of the genera Fucus and Ulva. In this study, we compared gene expression patterns of Idotea balthica individuals fed with Fucus vesiculosus to individuals fed with Ulva lactuca. We generated the frst-ever transcriptome assembly for this species, and found 3,233 diferentially expressed genes across feeding regimes. However, only a handful of biological functions were enriched with regard to diferentially expressed genes, the most notable being “alkaloid metabolic process”. Within this category, we found eight diferentially expressed cytochrome P450 (CYP) unigenes, all of which had a higher expression in the U. lactuca diet treatment. A phylogenetic analysis showed that the diferentially expressed CYP genes are closely related to a CYP gene described from the hepatopancreas of the spiny lobster Panulirus argus, and we hypothesize that these transcripts are involved in metabolite detoxifcation. This is a frst step in the understanding of this algae-grazer interaction, and will form a basis for future work to characterize cytochrome P450 functioning in marine crustaceans. Isopod crustaceans of the globally distributed genus Idotea are common in coastal marine areas. Tese species are generalist grazers on macroalgae and sea grasses, and can be ecologically important in structuring algal com- munities1. For example, in some areas in the Baltic Sea (Northern Europe), densities of Idotea balthica can rise to astonishing numbers (>80 individuals/100 g wet weight of the brown alga Fucus vesiculosus), which may tem- porarily cause a complete loss of F. vesiculosus in the area2. In areas with strong grazing pressure, algal genotypes with defensive strategies against grazing are favored by natural selection3. One common defense strategy among macrophytes is synthesis of secondary metabolites, which are bioactive compounds not directly related to growth or reproduction. In algae, these are ofen involved in grazer deterrence by decreasing the palatability of the tissue4. As some algal secondary metabolites have been found to have pharmaceutical applications, much research has been undertaken to gain a better understanding of these compounds5–9. As a result, a whole range of bioactive compounds have now been discovered in seaweeds10. However, the mechanism involved in grazer deterrence has been more difcult to conclusively elucidate to date. It has been suggested that the main grazer-deterring compounds in brown algae are polyphenolic com- pounds which have been named “phlorotannins”11,12. Tese compounds have the ability to bind to proteins and thus reduce the digestible nutrient content of the algae, while at the same time degrading the chemical environ- ment within the gut of the grazers. Jormalainen et al.13 observed that phlorotannin extracts reduced the assimi- lation efciency of I. balthica, but this did not deter the isopods from feeding. Other feeding trials with algae of varying phlorotannin concentrations have yielded mixed results, in some cases deterring grazing while in some cases actually stimulating feeding14. In green algae, such as the “sea lettuce” Ulva lactuca, dimethylsulfoniopropi- onate (DMSP) and acrylic acids15, as well as compounds producing reactive oxygen species (ROS)16 are induced 1University of Gothenburg, Department of Marine Sciences, Tjärnö, Sweden. 2University of Turku, Department of Biochemistry, Turku, Finland. Correspondence and requests for materials should be addressed to P.D.W. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:16824 | DOI:10.1038/s41598-018-34937-z 1 www.nature.com/scientificreports/ under grazing, and have been suggested to have a role in grazer deterrence and toxicity. ROS ingestion could cause oxidative damage in the guts of grazers, as has been shown in insects feeding of plant tissue17. However, while chemical defense compounds found in Ulva species caused sea urchin deterrence, they had the opposite efect on Idotea wosnesenskii15. In common periwinkles (Littorina spp.), a recent study found that the deterrence efects of Ulva lactuca were species-specifc, which the authors hypothesized could be due to diferences in feed- ing strategies (generalist vs specialist)18. As a consequence of the evolution of chemical defense compounds in the algae, it is expected that the grazers would evolve mechanisms for tolerance or detoxifcation of the algal compounds. A tolerance mechanism could act in diferent ways. For example, a highly efcient general detoxifcation mechanism for toxic compounds can be fne-tuned based on the diet. Tis would allow them to be generalists while still feeding on algal species with high quantities of secondary metabolites such as F. vesiculosus and U. lactuca. Common to all animals, the Cytochrome P450 (CYP) system is one of the major players in metabolism and detoxifcation of compounds produced by other organisms19–21. Cytochrome P450 is a superfamily of enzymes, consisting of several hundreds of diferent types which are classifed into diferent families22. Some of these have an important role in general metabolism and in development, while others are more involved in detoxifcation23. For example, CYP enzymes are induced in caterpillars afer being fed with nicotine-containing material24. In the marine environment, it has been shown that some variants of the CYP2 family, involved in detoxifcation of xenobiotic compounds, are present in the hepatopancreas of crustaceans25,26. While very few comparative studies have been conducted to date on crusta- cean CYP variants, it has been suggested that generalist algal grazers would beneft from the evolution of a high diversity of CYP genes27,28, as has been observed in the genome sequence of the purple urchin (Strongylocentrotus purpuratus)29. Each of these could then evolve an ability to metabolize a specifc group of compounds, generating a fnely-tuned diet-based detoxifcation machinery. In addition, it is possible that the isopods have acquired spe- cialized gut microbiota, which assist them in digesting toxic compounds before they are able to difuse from the gut into the tissues of the animal. In terrestrial isopods with diets containing hard-to-digest compounds such as cellulose, it is well-known that the gut microbiota plays an important role in digestion30,31. Te functional roles of gut microbes in species of the genus Idotea have not yet been investigated, but there have been some studies of the overall microbiota indicating that isopods from diferent geographic areas and with diferent diets possess distinct microbiomes31,32. It is also possible that some of the functions usually performed by gut bacteria could have been transferred to the isopods themselves. For example, the lignocellulose metabolic machinery other- wise only present in bacteria and fungi, can be found also in the genomes of isopods of the wood-boring genus Limnoria33. In particular, the glycosyl hydrolase family 7 (GH7) has 3 representatives which are all expressed in the gut transcriptome of Limnoria quadripunctata34 suggesting horizontal gene transfer from symbiont to host33. We here present a study investigating the detoxifcation mechanism of algal defense compounds in I. balthica using an RNA sequencing approach. We conducted an experiment where individuals of I. balthica were fed with diferent algal diets - one brown alga (F. vesiculosus) which is a common diet item for these isopods, and one green alga (U. lactuca) which is not as common in the isopods’ habitat. Representing two evolutionarily distant groups of algae, it is likely that there are considerably diferences in metabolite structure among the two. Subsequently, we examined diferences in gene expression among individuals from the diferent diet treatments supported by a reference transcriptome assembled from a combination of all tissue types from one adult male I. balthica. Our hypothesis was that the I. balthica individuals would induce expression of diet-specifc detoxifcation enzymes, either through isopod-specifc detoxifcation compounds, or as a response within the Cytochrome P450 path- way. If the latter was the case, we predicted a diversity of diferent Cytochrome P450 forms in the transcriptome sequence of I. balthica, of which many would be diferentially expressed in diferent diet treatments, and that these would be similar in sequence to variants of Cytochrome P450 found in other marine algal grazers. Results Transcriptome Assembly and Annotation. Te total number of reads amounted to 296,173,922, out of which 262,020,548 remained afer quality-trimming. Rcorrector was able to correct 46,535,134 bases pre-assem- bly, and the in silico normalization yielded a fnal set of 10,099,252 read pairs which were used as input for the de novo assembly (Table 1). Te raw assembly was fltered using read evidence and presence of ORFs using TransRate, with a resulting output assembly of 40,122 transcripts in 30,147 unigenes, an N50 of 1,710 bp and a total length of 47,523,534 bp (Table 1). Mapping the reads of the reference individual back to the fltered assembly, 67% of the reads mapped (58% with high quality). TransDecoder could fnd 21,439 putative peptides encoded by the fltered assembly (Table 1). Te BUSCO analysis searched for 2,675 Arthropod single-copy orthologs in the assembly, and found 1,645 (61.5%). Only 46.3% of these were single-copy and complete, and the remainders were fragments (19.5%), duplicates (23.0%) or triplicates (11.2%) (Table 1), resulting from either assembly fragmentation or separate assembly of the two alleles. Te PANNZER annotation, using an arthropod database, yielded annotations for 10,655 out of the 40,122 transcripts, while a separate BLASTx to NCBI’s non-redundant protein database (nr) yielded annotations for 19,498 transcripts (Table 1; Supplementary Table 1).
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