Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

Belcaid, Mahdi; Casaburi, Giorgio; McAnulty, Sarah J.; Schmidbaur, Hannah; Suria, Andrea M.; Moriano‐Gutierrez, Silvia; Pankey, M. Sabrina; Oakley, Todd H.; Kremer, Natacha; Koch, Eric J.; Collins, Andrew J.; Nguyen, Hoan; Lek, Sai; Goncharenko-Foster, Irina; Minx, Patrick; Sodergren, Erica; Weinstock, George M.; Rokhsar, Daniel S.; McFall‐Ngai, Margaret J.; Simakov, Oleg; Foster, Jamie S.; Nyholm, Spencer V.

doi:10.1073/pnas.1817322116

Cited by 132 publications

(207 citation statements)

References 35 publications

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“…The large number of assembled transcripts is a common trait found in other de novo assembled transcriptomes of E. scolopes (43,44). Cephalopods are known to expand certain gene families (45,46). This feature, together with the high levels of heterozygosity and transcript editing (47) that are known to challenge assembly software (48), contributed to the high number of observed expressed transcripts.…”

Section: Resources For Analyses Of Symbiosis Effects On Host Gene Expmentioning

confidence: 99%

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Moriano‐Gutierrez

Koch

Bussan

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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The colonization of an animal's tissues by its microbial partners creates networks of communication across the host's body. We used the natural binary light-organ symbiosis between the squid Euprymna scolopes and its luminous bacterial partner, Vibrio fischeri, to define the impact of colonization on transcriptomic networks in the host. A night-active predator, E. scolopes coordinates the bioluminescence of its symbiont with visual cues from the environment to camouflage against moon and starlight. Like mammals, this symbiosis has a complex developmental program and a strong day/night rhythm. We determined how symbiont colonization impacted gene expression in the light organ itself, as well as in two anatomically remote organs: the eye and gill. While the overall transcriptional signature of light organ and gill were more alike, the impact of symbiosis was most pronounced and similar in light organ and eye, both in juvenile and adult animals. Furthermore, the presence of a symbiosis drove daily rhythms of transcription within all three organs. Finally, a single mutation in V. fischeri-specifically, deletion of the lux operon, which abrogates symbiont luminescence-reduced the symbiosis-dependent transcriptome of the light organ by two-thirds. In addition, while the gills responded similarly to light-organ colonization by either the wildtype or mutant, luminescence was required for all of the colonizationassociated transcriptional responses in the juvenile eye. This study defines not only the impact of symbiont colonization on the coordination of animal transcriptomes, but also provides insight into how such changes might impact the behavior and ecology of the host. squid-vibrio | symbiosis | development | daily rhythm | bioluminescence

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Section: Resources For Analyses Of Symbiosis Effects On Host Gene Expmentioning

confidence: 99%

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Moriano‐Gutierrez

Koch

Bussan

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…A recent study of the Hawaiian bobtail squid ( Euprymna scolopes ), has shown that its light organ (LO), a specialized symbiotic structure that houses luminescent bacteria, expresses tandemly duplicated genes (i.e., reflectins) . Another symbiotic organ present in many squid species, the accessory nidamental gland (ANG), was found to be enriched in novel genes . Same scenario was found for other tissues, such as suckers of Octopus bimaculoides .…”

Section: Cephalopods: Model Systems For the Study Of Genome Evolutionmentioning

confidence: 94%

“…Only recently could genomic studies of cephalopods be accomplished . Large and repetitive genomes were hindering sequencing and assembly .…”

Section: Cephalopods: Model Systems For the Study Of Genome Evolutionmentioning

confidence: 99%

“…RNA editing was found to underlie temperature adaptation in potassium channels in polar octopuses and to be enriched in transcripts expressed in nervous tissues, similar to vertebrates . Finally, genome rearrangements at the coleoid ancestor split conserved gene clusters found across different metazoan levels (e.g., molluscs, lophotrochozoan, bilaterians) possibly providing novel cephalopod‐specific gene regulatory domains …”

Section: Cephalopods: Model Systems For the Study Of Genome Evolutionmentioning

confidence: 99%

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Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

et al. 2019

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How genomic innovation translates into organismal organization remains largely unanswered. Possessing the largest invertebrate nervous system, in conjunction with many species-specific organs, coleoid cephalopods (octopuses, squids, cuttlefishes) provide exciting model systems to investigate how organismal novelties evolve. However, dissecting these processes requires novel approaches that enable deeper interrogation of genome evolution. Here, the existence of specific sets of genomic co-evolutionary signatures between expanded gene families, genome reorganization, and novel genes is posited. It is reasoned that their co-evolution has contributed to the complex organization of cephalopod nervous systems and the emergence of ecologically unique organs. In the course of reviewing this field, how the first cephalopod genomic studies have begun to shed light on the molecular underpinnings of morphological novelty is illustrated and their impact on directing future research is described. It is argued that the application and evolutionary profiling of evolutionary signatures from these studies will help identify and dissect the organismal principles of cephalopod innovations. By providing specific examples, the implications of this approach both within and beyond cephalopod biology are discussed.

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“…[27,46,92,104,105,107,108]), nemerteans [89], molluscs (e.g. [30,36,41,92,107,[109][110][111][112]) and possibly kamptozoans [113] (however, in the latter the lox2-like sequence lacks most of the residues considered as lox2 signature; Additional file 1: Fig. S1).…”

Section: Hox Gene Complement In Phoronidamentioning

confidence: 99%

Hox gene expression during development of the phoronid Phoronopsis harmeri

Gąsiorowski

Hejnol

2020

EvoDevo

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Background: Phoronida is a small group of marine worm-like suspension feeders, which together with brachiopods and bryozoans form the clade Lophophorata. Although their development is well studied on the morphological level, data regarding gene expression during this process are scarce and restricted to the analysis of relatively few transcription factors. Here, we present a description of the expression patterns of Hox genes during the embryonic and larval development of the phoronid Phoronopsis harmeri. Results:We identified sequences of eight Hox genes in the transcriptome of Ph. harmeri and determined their expression pattern during embryonic and larval development using whole mount in situ hybridization. We found that none of the Hox genes is expressed during embryonic development. Instead their expression is initiated in the later developmental stages, when the larval body is already formed. In the investigated initial larval stages the Hox genes are expressed in the non-collinear manner in the posterior body of the larvae: in the telotroch and the structures that represent rudiments of the adult worm. Additionally, we found that certain head-specific transcription factors are expressed in the oral hood, apical organ, preoral coelom, digestive system and developing larval tentacles, anterior to the Hox-expressing territories. Conclusions:The lack of Hox gene expression during early development of Ph. harmeri indicates that the larval body develops without positional information from the Hox patterning system. Such phenomenon might be a consequence of the evolutionary intercalation of the larval form into an ancestral life cycle of phoronids. The observed Hox gene expression can also be a consequence of the actinotrocha representing a "head larva", which is composed of the most anterior body region that is devoid of Hox gene expression. Such interpretation is further supported by the expression of head-specific transcription factors. This implies that the Hox patterning system is used for the positional information of the trunk rudiments and is, therefore, delayed to the later larval stages. We propose that a new body form was intercalated to the phoronid life cycle by precocious development of the anterior structures or by delayed development of the trunk rudiment in the ancestral phoronid larva.

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Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

Cited by 132 publications

References 35 publications

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

Hox gene expression during development of the phoronid Phoronopsis harmeri

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