Mechanisms of Maternal Inheritance of Dinoflagellate Symbionts in the Acoelomorph WormWaminoa litus

Abstract

Waminoa litus is a zooxanthella-bearing acoel worm that infests corals. It is unique to Bilateria in that it transmits its algal symbionts vertically via eggs irrespective of the heterogeneity of the symbionts. It simultaneously harbors two dinoflagellate genera: Symbiodinium and Amphidinium. In this study, we examined the timing and vertical transmission pathway of algal symbionts in W. litus using light and electron microscopy. The oogenesis of the worm can be divided into three stages: stage I, in which the ovary is absent; stage II, the early vitellogenic zone containing immature oocytes formed in the ovary; and stage III, with both early and late vitellogenic zones in the body. In the early vitellogenic zone at stage II, oocytes are surrounded by accessory-follicle cells (AFCs). Both Symbiodinium and Amphidinium symbionts are not initially observed in the oocytes, but are observed in the AFCs. In the late vitellogenic zone at stage III, oocytes are enveloped by a complete sheath of AFCs; the algal symbionts are taken up by the late vitellogenic oocytes. These observations suggest that AFCs mediate the transfer of the algae from the parent to the oocytes. Ribotype analyses of the Symbiodinium symbionts revealed that they differ from those harbored by coral in the same experimental aquarium. These results indicate that W. litus has an active algal transport pathway and maintains a specific lineage of Symbiodinium via vertical transmission.

A Flatworm from the GenusWaminoa(Acoela: Convolutidae) Associated with Bleached Corals in Western Australia

“…As noted in other studies (Barneah et al, 2012;Hikosaka-Katayama et al, 2012), the non-specific binding of the nested 18S rDNA primers resulted in amplification of coral, fungal, and algal sequences (data not shown). As the 18S rDNA gene is highly conserved in animals, the differences between flatworm, coral, and symbiont 18S rDNA sequences is expected to be small.…”

“…For example, Barneah et al (2012) amplified coral and algal 18S rDNA sequences in addition to those of Waminoa when using primers designed by Norén and Jondelius (1999) for acoel flatworms, and noted the need for primers that specifically target Waminoa. Similarly, Hikosaka-Katayama et al (2012) recovered 18S rDNA sequences from the dinoflagellate Amphidinium while using these same primers to amplify flatworm DNA.…”

Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

“…While a large diversity of nudibranchs (mainly aeolids) are known to associate with Symbiodinium, there is a scarcity of larval experiments, possibly due to their typically restricted diet (Dionísio et al, 2013). The only exception is Berghia stephanieae, Bythell et al, 1997;Schwarz et al, 2002;Hambleton et al, 2014Alcyonacea Vertical and horizontal Planula No Benayahu et al, 1988, 1992Achituv et al, 1992;Slattery et al, 1999;Barneah et al, 2004 Scleractinia Vertical andhorizontal Planula No Weis et al, 2001;Marlow and Martindale, 2007;Harii et al, 2009;Mieog et al, 2009;Erwin and Szmant, 2010 Acoelomorpha Vertical Müller's larva n/a Barneah et al, 2007a,b;Hikosaka-Katayama et al, 2012 Mollusca Gastropoda Vertical and horizontal Veliger Yes b Kempf, 1984;Carroll and Kempf, 1990;Banaszak et al, 2013;Garcia Ramos and Banaszak, 2014;Wecker et al, 2015 Bivalvia Horizontal Veliger and pediveliger Fitt and Trench, 1981;Fitt et al, 1984Fitt et al, , 1986Heslinga et al, 1984Heslinga et al, , 1990Mies et al, 2012 a In the case of Aiptasia sp. ; unknown for other anemones.…”

Biology of Symbiotic Dinoflagellates (Symbiodinium) in Corals

“…In vertical transmission, Symbiodinium cells are directly inherited via the egg (Hirose and Hidaka 2006 ;Hikosaka-Katayama et al 2012 ), therefore this acquisition mode guarantees inheritance of maternal-compatible symbionts. However, horizontal transmission is rather common among animals.…”

“…Symbiodinium , recognized as a gymnodinioid dinofl agellate, is a major group of zooxanthellae in invertebrates and protozoan symbiosis, and is the most well studied. Of note, the Acoelomorph worm, Waminoa litus , harbors both Amphidinium and Symbiodinium simultaneously (Hikosaka-Katayama et al 2012 ). Kawaguti ( 1944 ) was the fi rst to observe that symbiotic zooxanthellae of the reef coral Acropora corymbosa produce motile gymnodinioid-like swarmers when isolated from their host coral, confi rming those symbionts as having dinofl agellate affi nities.…”