Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa

Clavijo, Jenny Melo; Frankenbach, Silja; Fidalgo, Cátia; Serôdio, João; Donath, Alexander; Preisfeld, Angelika; Christa, Gregor

doi:10.1002/ece3.6865

Cited by 16 publications

(22 citation statements)

References 99 publications

(202 reference statements)

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“…In mice macrophages, semaphorin positively regulated phagocytosis and the inflammatory response after LPS treatment ( 72 ). In invertebrates, semaphorins are likely involved in detection and phagocytosis of photosymbionts [in cnidarians ( 73 ), in sea slugs ( 74 )]. Sponges rely on phagocytosis for food uptake while depending on differential recognition of their symbionts.…”

Section: Discussionmentioning

confidence: 99%

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panicea

2021

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The animal immune system mediates host-microbe interactions from the host perspective. Pattern recognition receptors (PRRs) and the downstream signaling cascades they induce are a central part of animal innate immunity. These molecular immune mechanisms are still not fully understood, particularly in terms of baseline immunity vs induced specific responses regulated upon microbial signals. Early-divergent phyla like sponges (Porifera) can help to identify the evolutionarily conserved mechanisms of immune signaling. We characterized both the expressed immune gene repertoire and the induced response to lipopolysaccharides (LPS) in Halichondria panicea, a promising model for sponge symbioses. We exposed sponges under controlled experimental conditions to bacterial LPS and performed RNA-seq on samples taken 1h and 6h after exposure. H. panicea possesses a diverse array of putative PRRs. While part of those PRRs was constitutively expressed in all analyzed sponges, the majority was expressed individual-specific and regardless of LPS treatment or timepoint. The induced immune response by LPS involved differential regulation of genes related to signaling and recognition, more specifically GTPases and post-translational regulation mechanisms like ubiquitination and phosphorylation. We have discovered individuality in both the immune receptor repertoire and the response to LPS, which may translate into holobiont fitness and susceptibility to stress. The three different layers of immune gene control observed in this study, - namely constitutive expression, individual-specific expression, and induced genes -, draw a complex picture of the innate immune gene regulation in H. panicea. Most likely this reflects synergistic interactions among the different components of immunity in their role to control and respond to a stable microbiome, seawater bacteria, and potential pathogens.

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Section: Discussionmentioning

confidence: 99%

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panicea

2021

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“…The mechanisms utilized by the slugs to selectively sequester plastids from the algae they consume remain uncertain, although recent studies have shown that in E. chlorotica it is an active process reminiscent of that observed for symbiotic algae and corals ( Chan et al , 2018 ). The slugs possibly rely on scavenger receptors and thrombospondin type 1 repeat proteins for plastid recognition ( Melo Clavijo et al , 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Genetic autonomy and low singlet oxygen yield support kleptoplast functionality in photosynthetic sea slugs

Havurinne

Handrich

Antinluoma

et al. 2021

Journal of Experimental Botany

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Elysia chlorotica is a kleptoplastic sea slug that preys on Vaucheria litorea, stealing its plastids which continue to photosynthesize for months inside the animal cells. We investigated the native properties of V. litorea plastids to understand how they withstand the rigors of photosynthesis in isolation. Transcription of specific genes in laboratory-isolated V. litorea plastids was monitored up to seven days. The involvement of plastid-encoded FtsH, a key plastid maintenance protease, in recovery from photoinhibition in V. litorea was estimated in cycloheximide-treated cells. In vitro comparison of V. litorea and spinach thylakoids was applied to investigate ROS formation in V. litorea. In comparison to other tested genes, the transcripts of ftsH and translation elongation factor EF-Tu (tufA) decreased slowly during incubation of isolated V. litorea plastids. Higher level of FtsH was also evident in cycloheximide-treated cells during recovery from photoinhibition. Charge recombination in PSII of V. litorea was found to be fine-tuned to produce only small quantities of singlet oxygen ( 1O2), and the plastids also contain ROS-protective compounds. Our results support the view that the genetic characteristics of the plastids themselves are crucial in creating a photosynthetic sea slug. The plastid’s autonomous repair machinery is likely enhanced by low 1O2 production and by elevated expression of FtsH in the plastids.

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“…The mechanisms utilized by the slugs to selectively sequester plastids from their prey algae remain uncertain, although recent studies have shown that in E. chlorotica it is an active process reminiscent of that observed for symbiotic algae and corals (Chan et al, 2018). The slugs possibly rely on scavenger receptors and thrombospondintype-1 repeat proteins for plastid recognition (Clavijo et al, 2020). The sacoglossan's ability to sequester plastids tends to distract attention from the unique features of the sequestered organelle, forming the second component of a photosynthetic slug system.…”

Section: Introductionmentioning

confidence: 99%

Genetic autonomy and low singlet oxygen yield support kleptoplast functionality in photosynthetic sea slugs

Havurinne

Handrich

Antinluoma

et al. 2021

Preprint

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Elysia chlorotica is a kleptoplastic sea slug that preys on Vaucheria litorea, stealing its plastids which then continue to photosynthesize for months inside the animal cells. We investigated the native properties of V. litorea plastids to understand how they withstand the rigors of photosynthesis in isolation. Transcription of specific genes in laboratory-isolated V. litorea plastids was monitored up to seven days. The involvement of plastid-encoded FtsH, a key plastid maintenance protease, in recovery from photoinhibition in V. litorea was estimated in cycloheximide-treated cells. In vitro comparison of V. litorea and spinach thylakoids was applied to investigate ROS formation in V. litorea. Isolating V. litorea plastids triggered upregulation of ftsH and translation elongation factor EF-Tu (tufA). Upregulation of FtsH was also evident in cycloheximide-treated cells during recovery from photoinhibition. Charge recombination in PSII of V. litorea was found to be fine-tuned to produce only small quantities of singlet oxygen (1O2). Our results support the view that the genetic characteristics of the plastids themselves are crucial in creating a photosynthetic sea slug. The plastid's autonomous repair machinery is likely enhanced by low 1O2 production and by upregulation of FtsH in the plastids.

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Identification of scavenger receptors and thrombospondin‐type‐1 repeat proteins potentially relevant for plastid recognition in Sacoglossa

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 16 publications

References 99 publications

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panicea

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panicea

Genetic autonomy and low singlet oxygen yield support kleptoplast functionality in photosynthetic sea slugs

Genetic autonomy and low singlet oxygen yield support kleptoplast functionality in photosynthetic sea slugs

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