Active host response to algal symbionts in the sea slug elysia chlorotica

Published on Jul 1, 2018in Molecular Biology and Evolution 10.22
· DOI :10.1093/molbev/msy061
Cheong Xin Chan19
Estimated H-index: 19
(University of Queensland),
Pavel Vaysberg2
Estimated H-index: 2
(Rutgers University)
+ 3 AuthorsDebashish Bhattacharya64
Estimated H-index: 64
(Rutgers University)
Abstract
Sacoglossan sea slugs offer fascinating systems to study the onset and persistence of algal-plastid symbioses. Elysia chlorotica is particularly noteworthy because it can survive for months, relying solely on energy produced by ingested plastids of the stramenopile alga Vaucheria litorea that are sequestered in cells lining its digestive diverticula. How this animal can maintain the actively photosynthesizing organelles without replenishment of proteins from the lost algal nucleus remains unknown. Here we used RNA-Seq analysis to test the idea that plastid sequestration leaves a significant signature on host gene expression during E. chlorotica development. Our results support this hypothesis and show that upon exposure to and ingestion of V. litorea plastids, genes involved in microbe-associated molecular patterns (MAMPs) and oxidative stress-response mechanisms are significantly up-regulated. Interestingly, our results with E. chlorotica mirror those found with corals that maintain dinoflagellates as intact cells in symbiosomes, suggesting parallels between these animal-algal symbiotic interactions.
  • References (14)
  • Citations (4)
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References14
Published on Dec 1, 2012in Symbiosis 1.71
Karen N. Pelletreau6
Estimated H-index: 6
(University of Maine),
Jared M. Worful4
Estimated H-index: 4
(University of Maine)
+ 1 AuthorsMary E. Rumpho7
Estimated H-index: 7
(University of Maine)
The kleptoplastic sacoglossan Elysia chlorotica shares a requisite, intracellular symbiosis with the plastids (= chloroplasts) of the Xanthophyte alga Vaucheria litorea. Although wild specimens have been used to address a range of biological questions, no studies have thoroughly characterized animal development during the initial establishment of the symbiosis under controlled laboratory conditions. Laboratory culture conditions were modified and the time required for successful metamorphosis wa...
11 Citations Source Cite
F. Giménez Casalduero4
Estimated H-index: 4
(University of Alicante),
C. Muniain2
Estimated H-index: 2
The importance of photosynthetic products derived from kleptoplasts in several sacoglossan species is being investigated in different fields, such as chemistry, biomolecular genetics and ecology. This study analyzes the effect of kleptoplasts on the survival rates of Elysia timida by evaluating the development of chlorophyll concentration, total length and survival rates of starved E. timida specimens kept in the light and in the dark. Although chlorophyll concentration values were similar in bo...
45 Citations Source Cite
Published on Nov 1, 2009in Molecular Plant 9.33
Mary E. Rumpho19
Estimated H-index: 19
(University of Maine),
Sirisha Pochareddy1
Estimated H-index: 1
(University of Maine)
+ 7 AuthorsKara M. Soule2
Estimated H-index: 2
(University of Maine)
Phosphoribulokinase (PRK), a nuclear-encoded plastid-localized enzyme unique to the photosynthetic carbon reduction (Calvin) cycle, was cloned and characterized from the stramenopile alga Vaucheria litorea. This alga is the source of plastids for the mollusc (sea slug) Elysia chlorotica which enable the animal to survive for months solely by photoautotrophic CO2 fixation. The 1633-bp V. litorea prk gene was cloned and the coding region, found to be interrupted by four introns, encodes a 405-amin...
33 Citations Source Cite
Julia A. Schwartzman10
Estimated H-index: 10
(University of Wisconsin-Madison),
Eric Koch5
Estimated H-index: 5
(University of Wisconsin-Madison)
+ 4 AuthorsEdward G. Ruby52
Estimated H-index: 52
(University of Wisconsin-Madison)
Abstract Glycans have emerged as critical determinants of immune maturation, microbial nutrition, and host health in diverse symbioses. In this study, we asked how cyclic delivery of a single host-derived glycan contributes to the dynamic stability of the mutualism between the squid Euprymna scolopes and its specific, bioluminescent symbiont, Vibrio fischeri. V. fischeri colonizes the crypts of a host organ that is used for behavioral light production. E. scolopes synthesizes the polymeric glyca...
25 Citations Source Cite
Published on Jan 15, 2011in The Journal of Experimental Biology 3.18
Mary E. Rumpho19
Estimated H-index: 19
,
Karen N. Pelletreau6
Estimated H-index: 6
+ 1 AuthorsDebashish Bhattacharya64
Estimated H-index: 64
Summary Symbiotic animals containing green photobionts challenge the common perception that only plants are capable of capturing the sun9s rays and converting them into biological energy through photoautotrophic CO 2 fixation (photosynthesis). ‘Solar-powered’ sacoglossan molluscs, or sea slugs, have taken this type of symbiotic association one step further by solely harboring the photosynthetic organelle, the plastid (=chloroplast). One such sea slug, Elysia chlorotica , lives as a ‘plant’ when ...
92 Citations Source Cite
Published on Apr 1, 2011in Plant Physiology 5.95
Karen N. Pelletreau6
Estimated H-index: 6
,
Debashish Bhattacharya64
Estimated H-index: 64
+ 3 AuthorsMary E. Rumpho7
Estimated H-index: 7
(University of Maine System)
[Trench (1969)][1] was the first to characterize the kleptoplastic (i.e. “stolen plastid”) relationship between the sacoglossan mollusc Elysia chlorotica and its algal prey ( Vaucheria litorea ). In contrast to E. chlorotica , which retains only the plastids of the alga in densely packed
43 Citations Source Cite
Published on May 14, 2014in PLOS ONE 2.77
Karen N. Pelletreau6
Estimated H-index: 6
(University of Connecticut),
Andreas P. M. Weber57
Estimated H-index: 57
+ 1 AuthorsMary E. Rumpho19
Estimated H-index: 19
The establishment of kleptoplasty (retention of ‘‘stolen plastids’’) in the digestive tissue of the sacoglossan Elysia chlorotica Gould was investigated using transmission electron microscopy. Cellular processes occurring during the initial exposure to plastids were observed in laboratory raised animals ranging from 1–14 days post metamorphosis (dpm). These observations revealed an abundance of lipid droplets (LDs) correlating to plastid abundance. Starvation of animals resulted in LD and plasti...
15 Citations Source Cite
Published on Jun 1, 2012in Microbiology and Molecular Biology Reviews 13.44
Simon K. Davy26
Estimated H-index: 26
(Victoria University of Wellington),
Denis Allemand2
Estimated H-index: 2
,
Virginia M. Weis35
Estimated H-index: 35
(Oregon State University)
Summary: The symbiosis between cnidarians (e.g., corals or sea anemones) and intracellular dinoflagellate algae of the genus Symbiodinium is of immense ecological importance. In particular, this symbiosis promotes the growth and survival of reef corals in nutrient-poor tropical waters; indeed, coral reefs could not exist without this symbiosis. However, our fundamental understanding of the cnidarian-dinoflagellate symbiosis and of its links to coral calcification remains poor. Here we review wha...
268 Citations Source Cite
Published on Aug 1, 2013in Molecular Biology and Evolution 10.22
Debashish Bhattacharya64
Estimated H-index: 64
(Rutgers University),
Karen N. Pelletreau6
Estimated H-index: 6
(University of Maine)
+ 2 AuthorsMary E. Rumpho7
Estimated H-index: 7
(University of Maine)
The sea slug Elysia chlorotica offers a unique opportunity to study the evolution of a novel function (photosynthesis) in a complex multicellular host. Elysia chlorotica harvests plastids (absent of nuclei) from its heterokont algal prey, Vaucheria litorea. The “stolen” plastids are maintained for several months in cells of the digestive tract and are essential for animal development. The basis of long-term maintenance of photosynthesis in this sea slug was thought to be explained by extensive h...
47 Citations Source Cite
Published on May 1, 2000in Plant Physiology 5.95
Mary E. Rumpho19
Estimated H-index: 19
,
Elizabeth J. Summer19
Estimated H-index: 19
,
James R. Manhart20
Estimated H-index: 20
Solar-powered “leaves that crawl”? This description of photosynthetic sea slugs (adapted from Bill Rudman [[www.austmus.gov.au/seaslugs/solarpow.htm][1]] and Robert Trench [1975]) aptly describes the symbiotic association that occurs between certain molluscan sea slugs and algal chloroplasts.
117 Citations Source Cite
Cited By4
Published on Nov 1, 2018in Biological Reviews 11.70
Jenny Melo Clavijo1
Estimated H-index: 1
,
Alexander Donath13
Estimated H-index: 13
+ 1 AuthorsGregor Christa9
Estimated H-index: 9
(University of Aveiro)
2 Citations Source Cite
Published on Jan 23, 2019in Symbiosis 1.71
Klara Scharnagl3
Estimated H-index: 3
(Michigan State University)
At the 2018 International Symbiosis Society Congress research was shared on symbioses across a wide variety of scales, from the temporal to the spatial, and from the very small to the very large. Advances in our technologies and computational abilities have enabled us to probe deeper than ever before into the nature of symbiosis, revealing a tremendous diversity, novel associations, and a deeper understanding of the initiation and maintenance of symbioses over time. Researchers at ISSC 2018 also...
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Published on Feb 19, 2019in Scientific Data 5.31
Huimin Cai1
Estimated H-index: 1
,
Qiye Li18
Estimated H-index: 18
+ 15 AuthorsJulie A. Schwartz8
Estimated H-index: 8
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