Innate immunity and cnidarian-Symbiodiniaceae mutualism

Mansfield, Katelyn M.; Gilmore, Thomas D.

doi:10.1016/j.dci.2018.09.020

Cited by 68 publications

(92 citation statements)

References 118 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…For example, immune processes such as neurotransmitter binding, transcription regulation, cellular communication, and biological adhesion, were only regulated after the MOB challenge, while scavenger receptor activity, hormone metabolic processes, and cell killing were vigorously modulated after the V. alginolyticus challenge. These ndings con rmed the involvement of cell communication and cell adhesion in Bathymodiolinae symbiosis, which could also be observed in holobionts such as coral and squid [2,[43][44][45]. Comparatively, scavenger receptor activity and cell killing were also well known in pathogen induced immune response with indispensable role in the elimination of pathogens [44][45][46][47].…”

Section: Global Immune Response Of Gigantidas Against Mobs and Nonsymsupporting

confidence: 52%

microRNAs Facilitate Comprehensive Responses of Bathymodiolinae Mussel Against Symbiotic and Nonsymbiotic Bacteria Stimulation

Chen

Wang

Zhang

et al. 2020

Preprint

View full text Add to dashboard Cite

Background:As the dominant species inhabiting both cold seeps and hydrothermal vents,Bathymodiolinae mussels are one of the most successful megafauna in the deep sea.They thrive in dark and food-insufficient environmentsby harboring sulfur-oxidizing bacteria (SOB)and/or methane-oxidizing bacteria (MOB)ingill bacteriocytesand obtain the majority of their nutrition from them.Many attempts have been made to decode the mechanisms underlying their symbiosis, which yetremained largely undisclosedfor years due to the lack of cultivable symbionts. In the present study,the globalexpression pattern of immune-related genes and miRNAswere surveyed inGigantidasplatifronsduring bacterial challengesusing enriched symbiontsor nonsymbioticVibrio in attempting to reveal the molecular mechanisms underlying chemosynthetic symbiosis. Results: Multiple PRRs such as TLRs, LRRs and C1q were found vigorously modulated during challenges whiledistinctly clusteredbetween symbiotic and nonsymbiotic bacteria stimulation. As downstream of the immune response,dozens of immune effectors including HSP70, P450, CD82 andvacuolar protein sorting-associated proteinwere modulated simultaneously, contributing to the fine tuning of cellular homeostasis, lysosome activity and bacteria engulfment in either symbiotic and nonsymbiotic bacteria challenge.A total of 459 miRNAs were identified in gill tissue of G. platifrons while dozens of themwere differentially expressedduring the challenge.Among these miRNAs, some were also found in differentexpression patternbetween symbiont or nonsymbiontchallenges and targeting apoptosis and phagosome maturation-related genes, including caspase8, inhibitor of apoptosis, cAMP-responsive element-binding protein,IκB, Rab and integrin. Conclusion:It was suggested that G. platifrons PRRs might function cooperativelyto facilitate the specialized immune recognition to MOBs or nonsymbioticbacteria. Meanwhile, a shared expression pattern of immune effectorswas observed between bacterial challenges, indicatingthe conservative response of Bathymodiolinae mussels in promoting the adhesion andengulfment of symbionts and nonsymbiont. Nevertheless, the differentially expressed miRNAs were yet suggested to facilitate specialized modulationinsymbiosis by repressing apoptosis- and phagosome maturation-related genes.With the orchestra of immune-related genes and miRNAs, G. platifronsmussels could therefore maintain arobust immune response against invading pathogens while establishing symbiosis with chemosynthetic bacteria.

show abstract

Section: Global Immune Response Of Gigantidas Against Mobs and Nonsymsupporting

confidence: 52%

microRNAs Facilitate Comprehensive Responses of Bathymodiolinae Mussel Against Symbiotic and Nonsymbiotic Bacteria Stimulation

Chen

Wang

Zhang

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Colonization by beneficial symbionts might lead to the suppression of the host immune response, or symbionts have evolved ways to avoid the host immune response. Similar mechanisms occur in other symbioses, such as squid and Aliivibrio fischeri 30 ; rhizobia, which are the nitrogen-fixing bacteria inside the root nodules of legumes 31 ; and sea anemones and dinoflagellate algae 32 . Thus, the acquisition of a diverse bacterial community in early life may be possible because the coral has not yet developed a fully functional immune system 33 .…”

Section: [H1] Space Time and Host-specificitymentioning

confidence: 77%

Coral microbiome dynamics, functions and design in a changing world

2019

View full text Add to dashboard Cite

Corals associate not only with dinoflagellates, which are their algal endosymbionts and which have been extensively studied over the past four decades, but also with a diversity of other microbes. The coral microbiome includes the dinoflagellates, viruses, fungi, archaea and bacteria, with knowledge of the last growing rapidly. This Review focuses on the bacterial members of the coral microbiome and draws parallels with better-studied microbiomes in other biological systems. We synthesize current understanding of spatial, temporal and host-specific patterns in coral-associated bacterial communities, the drivers shaping these patterns and the role of the microbiome in acclimatization and adaptation of the host to climate warming. We discuss how this knowledge can be harnessed to assist the future persistence of coral reefs and provide novel perspectives for the development of microbiome engineering and its implications for coral reef conservation and restoration.

show abstract

“…As the sister group to bilaterians, cnidarians have a complex innate immune system that is implicated in recognising pathogens and managing beneficial microorganisms, including endosymbionts. Previous transcriptomic analyses comparing aposymbiotic to symbiotic Aiptasia larvae and adult animals revealed several immune-related genes to be downregulated in response to symbiosis (reviewed in Mansfield and Gilmore, 2018). Specifically, symbionts have been proposed to induce immune suppression through NF-κB downregulation, possibly via TGFbsignalling (Berthelier et al, 2017;Detournay et al, 2012;Mansfield et al, 2019Mansfield et al, , 2017.…”

Section: Symbiosis Establishment Broadly Suppresses Host Cell Immunitmentioning

confidence: 99%

Dinoflagellate symbionts escape vomocytosis by host cell immune suppression

Jacobovitz

Rupp

Voss

et al. 2019

Preprint

View full text Add to dashboard Cite

Emergence of the symbiotic lifestyle fostered the immense diversity of all ecosystems on Earth, but symbiosis plays a particularly remarkable role in marine ecosystems. Photosynthetic dinoflagellate endosymbionts power reef ecosystems by transferring vital nutrients to their coral hosts. The mechanisms driving this symbiosis, specifically those which allow hosts to discriminate between beneficial symbionts and pathogens, are not well understood. Here, we uncover that host immune suppression is key for dinoflagellate endosymbionts to avoid elimination by the host using a comparative, model systems approach. Unexpectedly, we find that the clearance of nonsymbiotic microalgae occurs by non-lytic expulsion (vomocytosis) and not intracellular digestion, the canonical mechanism used by professional immune cells to destroy foreign invaders. We provide evidence that suppression of TLR signalling by targeting the conserved MyD88 adapter protein has been co-opted for this endosymbiotic lifestyle, suggesting that this is an evolutionarily ancient mechanism exploited to facilitate symbiotic associations ranging from coral endosymbiosis to the microbiome of vertebrate guts. Main Text SummarySymbiotic interactions appear in all domains of life and are key drivers of adaption and evolutionary diversification. A prime example is the endosymbiosis between corals and eukaryotic, photosynthetic dinoflagellates, which the hosts take up from the environment by phagocytosis.Once intracellular, endosymbionts transfer vital nutrients to the corals, a process fundamental for survival in nutrient-poor environments (Muscatine, 1990;Yellowlees et al., 2008). A central question is how endosymbionts circumvent the hosts' defensive strategies to persist intracellularly and conversely, how hosts prevent invasion by non-symbiotic microorganisms. Here, we use a comparative approach in the anemone model Exaiptasia pallida (commonly Aiptasia) (Hambleton et al., 2019;Tolleter et al., 2013;Weis et al., 2008) to address this. Using RNA-seq, we show that symbiont phagocytosis leads to a broad scale, cell-specific transcriptional suppression of host innate immunity, but phagocytosis of non-symbiotic microalgae does not. We show that targeting MyD88 to inhibit canonical TLR signalling promotes symbiosis establishment. Using live imaging and chemical perturbations, we demonstrate that non-symbiotic microalgae are cleared from the host by ERK5-dependent vomocytosis (non-lytic expulsion) (Alvarez and Casadevall, 2006;Gilbert et al., 2017;Ma et al., 2006), and that immune suppression is key for symbiont persistence and for establishment of an intracellular LAMP1 niche. We propose that expulsion is a fundamental mechanism of ancient innate immunity used to eliminate foreign cells; a process that is subverted by symbionts in the endosymbiotic association that forms the foundation of coral reef ecosystems. University) Postdoctoral Program, and a PhD scholarship within the Graduate School "Evolutionary Novelty & Adaptation by the Baden-Württemberg Landesgraduier...

show abstract

Innate immunity and cnidarian-Symbiodiniaceae mutualism

Cited by 68 publications

References 118 publications

microRNAs Facilitate Comprehensive Responses of Bathymodiolinae Mussel Against Symbiotic and Nonsymbiotic Bacteria Stimulation

microRNAs Facilitate Comprehensive Responses of Bathymodiolinae Mussel Against Symbiotic and Nonsymbiotic Bacteria Stimulation

Coral microbiome dynamics, functions and design in a changing world

Dinoflagellate symbionts escape vomocytosis by host cell immune suppression

Contact Info

Product

Resources

About