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

Published on Jul 1, 2018in Molecular Biology and Evolution 14.80
· DOI :10.1093/molbev/msy061
Cheong Xin Chan19
Estimated H-index: 19
(UQ: University of Queensland),
Pavel Vaysberg2
Estimated H-index: 2
(RU: Rutgers University)
+ 3 AuthorsDebashish Bhattacharya64
Estimated H-index: 64
(RU: Rutgers University)
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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
Newest
Published on Dec 1, 2017in Scientific Reports 4.01
Felisa Rey5
Estimated H-index: 5
(University of Aveiro),
Elisabete da Costa6
Estimated H-index: 6
(University of Aveiro)
+ 6 AuthorsSónia Cruz13
Estimated H-index: 13
(University of Aveiro)
Sacoglossan sea slugs, also known as crawling leaves due to their photosynthetic activity, are highly selective feeders that incorporate chloroplasts from specific macroalgae. These “stolen” plastids - kleptoplasts - are kept functional inside animal cells and likely provide an alternative source of energy to their host. The mechanisms supporting the retention and functionality of kleptoplasts remain unknown. A lipidomic mass spectrometry-based analysis was performed to study kleptoplasty of the...
2 Citations Source Cite
Published on Dec 1, 2017in Scientific Reports 4.01
Paulo Cartaxana18
Estimated H-index: 18
(University of Aveiro),
Erik Trampe7
Estimated H-index: 7
(UCPH: University of Copenhagen)
+ 1 AuthorsSónia Cruz13
Estimated H-index: 13
(University of Aveiro)
Several sacoglossan sea slug species feed on macroalgae and incorporate chloroplasts into tubular cells of their digestive diverticula. We investigated the role of the “stolen” chloroplasts (kleptoplasts) in the nutrition of the sea slug Elysia viridis and assessed how their abundance, distribution and photosynthetic activity were affected by light and starvation. Elysia viridis individuals feeding on the macroalga Codium tomentosum were compared with starved specimens kept in dark and low light...
5 Citations Source Cite
Published on Jul 1, 2016in Molecular Ecology 5.86
A. R. Mohamed1
Estimated H-index: 1
,
Vivian R. Cumbo13
Estimated H-index: 13
(JCU: James Cook University)
+ 8 AuthorsNoriyuki Satoh47
Estimated H-index: 47
(OIST: Okinawa Institute of Science and Technology)
Despite the ecological significance of the relationship between reef-building corals and intracellular photosynthetic dinoflagellates of the genus Symbiodinium, very little is known about the molecular mechanisms involved in its establishment. Indeed, microarray-based analyses point to the conclusion that host gene expression is largely or completely unresponsive during the establishment of symbiosis with a competent strain of Symbiodinium. In this study, the use of Illumina RNA-Seq technology a...
30 Citations Source Cite
Julia A. Schwartzman10
Estimated H-index: 10
(UW: University of Wisconsin-Madison),
Eric Koch5
Estimated H-index: 5
(UW: University of Wisconsin-Madison)
+ 4 AuthorsEdward G. Ruby53
Estimated H-index: 53
(UW: 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...
27 Citations Source Cite
Published on May 14, 2014in PLOS ONE 2.78
Karen N. Pelletreau3
Estimated H-index: 3
(UConn: University of Connecticut),
Andreas P. M. Weber58
Estimated H-index: 58
+ 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 Nov 20, 2013
Gregor Christa11
Estimated H-index: 11
,
Verena Zimorski9
Estimated H-index: 9
(HHU: University of Düsseldorf)
+ 4 AuthorsSven B. Gould24
Estimated H-index: 24
(HHU: University of Düsseldorf)
Several sacoglossan sea slugs (Plakobranchoidea) feed upon plastids of large unicellular algae. Four species—called long-term retention (LtR) species—are known to sequester ingested plastids within specialized cells of the digestive gland. There, the stolen plastids (kleptoplasts) remain photosynthetically active for several months, during which time LtR species can survive without additional food uptake. Kleptoplast longevity has long been puzzling, because the slugs do not sequester algal nucl...
31 Citations Source Cite
Published on Aug 1, 2013in Molecular Biology and Evolution 14.80
Debashish Bhattacharya64
Estimated H-index: 64
(RU: Rutgers University),
Karen N. Pelletreau3
Estimated H-index: 3
(UMaine: University of Maine)
+ 2 AuthorsMary E. Rumpho6
Estimated H-index: 6
(UMaine: 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 Dec 1, 2012in Symbiosis 2.01
Karen N. Pelletreau3
Estimated H-index: 3
(UMaine: University of Maine),
Jared M. Worful4
Estimated H-index: 4
(UMaine: University of Maine)
+ 1 AuthorsMary E. Rumpho6
Estimated H-index: 6
(UMaine: 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
Published on Jun 1, 2012in Microbiology and Molecular Biology Reviews 15.26
Simon K. Davy27
Estimated H-index: 27
(Victoria University of Wellington),
Denis Allemand2
Estimated H-index: 2
,
Virginia M. Weis35
Estimated H-index: 35
(OSU: 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...
277 Citations Source Cite
Published on Apr 1, 2011in Plant Physiology 6.30
Karen N. Pelletreau6
Estimated H-index: 6
,
Debashish Bhattacharya64
Estimated H-index: 64
+ 3 AuthorsMary E. Rumpho1
Estimated H-index: 1
(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
Cited By4
Newest
Published on Jan 23, 2019in Symbiosis 2.01
Klara Scharnagl3
Estimated H-index: 3
(MSU: 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
Huimin Cai1
Estimated H-index: 1
,
Qiye Li18
Estimated H-index: 18
+ 15 AuthorsJulie A. Schwartz8
Estimated H-index: 8
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Published on Nov 1, 2018in Biological Reviews 10.29
Jenny Melo Clavijo1
Estimated H-index: 1
,
Alexander Donath13
Estimated H-index: 13
+ 1 AuthorsGregor Christa11
Estimated H-index: 11
(University of Aveiro)
2 Citations Source Cite