Heat Stress-Activated, Calcium-Dependent Nitric Oxide Synthase in Sponges

doi:10.1006/niox.2001.0366

Nitric Oxide

Volume 5, Issue 5, October 2001, Pages 427-431

https://doi.org/10.1006/niox.2001.0366 Get rights and content

Abstract

The presence of Ca²⁺-dependent, heat-stress-activated nitric oxide synthase (NOS) activity in peculiarly shaped, fusiform, and dendritic sponge cells is described for the first time. The NOS activity was evidenced evaluating the conversion of radioactive citrulline from [¹⁴C]arginine in intact cells from two different species that are phylogenetically unrelated in the class of Demospongiae: Axinella polypoides and Petrosia ficiformis. The production of nitrogen monoxide (NO) was confirmed by electron paramagnetic resonance analysis, and the histochemistry technique of NADPH diaphorase showed a specific localization of NOS activity in a particular network of dendritic cells in the sponge parenchyma. Sponges are the most primitive metazoan group; their evolution dates back 600 million years. The presence of environmental stress-activated NOS activity in these organisms may prove to be the most ancient NO-dependent signaling network in the animal kingdom.

References (16)

Z.S. Li et al.
Relationships between nitric oxide synthase, vasoactive intestinal peptide and substance P immunoreactivities in neurons of the amphibian intestine
J. Auton. Nerv. Syst.
(1993)
S. Haverkamp et al.
Endothelial nitric oxide synthase (eNOS) is localized to Muller cells in all vertebrate retinas
Vision Res.
(1999)
V.B. Kumar et al.
Rapid assay for nitric oxide synthase using thin-layer chromatography
Anal. Biochem.
(1999)
V.D. Mikoyan et al.
The influence of antioxidants and cycloheximide on the level of nitric oxide in the livers of mice in vivo
Biochim. Biophys. Acta
(1995)
T. Matsumoto et al.
A correlation between soluble brain nitric oxide synthase and NADPH–diaphorase activity is only seen after exposure of the tissue to fixative
Neurosci. Lett.
(1993)
D.S. Bredt et al.
Nitric oxide: A physiologic messenger molecule
Annu. Rev. Biochem.
(1994)
T. Michel et al.
Nitric oxide synthases: Which, where, how, and why?
J. Clin. Invest.
(1997)

There are more references available in the full text version of this article.

Cited by (37)

Diversity and functional roles of the symbiotic microbiome associated to marine sponges off Karah Island, Terengganu, Malaysia
2023, Regional Studies in Marine Science
Marine sponges harbor a complex microbial consortium that plays important roles in host metabolisms and the production of chemical compounds. Symbiotic microbial community structures of marine sponges have been studied in recent years especially in the Caribbean and the Mediterranean Sea, whereas there is still a paucity of research in Malaysia. This study investigated the microbial community structures associated with four different marine sponge species (Aaptos suberitoides (Brøndsted, 1934), Neopetrosia exigua (Kirkpatrick, 1900), Theonella swinhoei (Gray, 1868), and Xestospongia testudinaria (Lamarck, 1815)) collected from Karah Island, Peninsular Malaysia. Microbial genomic DNA of four sponges and surrounding seawater were extracted and 16S rRNA gene amplicon sequencing was conducted targeting V3–V4 variable region using Illumina MiSeq platform. Paired-end sequences were analyzed using QIIME2 and the potential microbial functions related to the microbial communities of marine sponges and seawater were annotated using functional annotation of prokaryotic taxa (FAPROTAX). Microbial community structures and compositions were clearly different between sponges and seawater, as well as within different sponge species. Taxonomic analysis showed that Chloroflexi was the predominant phylum in all sponge species. Proteobacteria and Actinobacteriota were composing the core taxa of the microbial communities in N. exigua, T. swinhoei, and X. testudinaria, whereas Cyanobacteria and Proteobacteria were dominant in A. suberitoides. The functional analysis revealed that the abundance of the “predatory or exoparasitic” function was high in all sponges. The functions of aerobic ammonia oxidation and nitrification were dominant in marine sponges, rather than seawater. This study has important implications in understanding the microbial community structures associated with marine sponges in Malaysia, and gives fundamental information of sponge–microbe interactions and functional roles for future investigations.
Nitric oxide signaling controls collective contractions in a colonial choanoflagellate
2022, Current Biology
Citation Excerpt :
These results further support the existence of NO/cGMP signaling in C. flexa and is consistent with it being mediated (at least in part) by Cf sGC1. In animals, NO signaling can be induced by a broad range of stimuli, which include chemical signals (for example, acetylcholine in mammalian blood vessels35), mechanical cues (for example, shear stress in blood vessels36), or heat shocks.37–40 Interestingly, collar contractions in choanoflagellates can often be induced by mechanical stimuli, such as flow and touch.41–44
Although signaling by the gaseous molecule nitric oxide (NO) regulates key physiological processes in animals, including contractility,1, 2, 3 immunity,⁴^,⁵ development,6, 7, 8, 9 and locomotion,¹⁰^,¹¹ the early evolution of animal NO signaling remains unclear. To reconstruct the role of NO in the animal stem lineage, we set out to study NO signaling in choanoflagellates, the closest living relatives of animals.¹² In animals, NO produced by the nitric oxide synthase (NOS) canonically signals through cGMP by activating soluble guanylate cyclases (sGCs).¹³^,¹⁴ We surveyed the distribution of the NO signaling pathway components across the diversity of choanoflagellates and found three species that express NOS (of either bacterial or eukaryotic origin), sGCs, and downstream genes previously shown to be involved in the NO/cGMP pathway. One of the species coexpressing sGCs and a bacterial-type NOS, Choanoeca flexa, forms multicellular sheets that undergo collective contractions controlled by cGMP.¹⁵ We found that treatment with NO induces cGMP synthesis and contraction in C. flexa. Biochemical assays show that NO directly binds C. flexa sGC1 and stimulates its cyclase activity. The NO/cGMP pathway acts independently from other inducers of C. flexa contraction, including mechanical stimuli and heat, but sGC activity is required for contractions induced by light-to-dark transitions. The output of NO signaling in C. flexa—contractions resulting in a switch from feeding to swimming—resembles the effect of NO in sponges1, 2, 3 and cnidarians,¹¹^,¹⁶^,¹⁷ where it interrupts feeding and activates contractility. These data provide insights into the biology of the first animals and the evolution of NO signaling.
Transcriptional changes of Pacific oyster Crassostrea gigas reveal essential role of calcium signal pathway in response to CO<inf>2</inf>-driven acidification
2020, Science of the Total Environment
Citation Excerpt :
Its products NO can directly or indirectly modulate the activity of Ca2+ channels or can rapidly react with O2− (Mazars et al., 2010). Compared with vertebrate, there is only one NOS in C. gigas (Jiang et al., 2016), and the invertebrate NOS was reported to respond to a variety of environmental stresses such as heat, pollution, pH, bacteria and air exposure (Chen, 2017; Giovine et al., 2001; Jiang et al., 2013; Novas et al., 2007; Smith et al., 2000). Therefore these altered mRNA/protein expressions could provide an explanation for the reduced oxidative stresses to long-term CO2 exposure.
There is increasing evidence that ocean acidification (OA) has a significant impact on marine organisms. However, the ability of most marine organisms to acclimate to OA and the underlying mechanisms are still not well understood. In the present study, whole transcriptome analysis was performed to compare the impacts of short- (7 days, named as short group) and long- (60 days, named as long group) term CO₂ exposure (pH 7.50) on Pacific oyster Crassostrea gigas. The responses of C. gigas to short- and long-term CO₂ exposure shared common mechanisms in metabolism, membrane-associated transportation and binding processes. Long-term CO₂ exposure induced significant expression of genes involved in DNA or RNA binding, indicating the activated transcription after long-term CO₂ exposure. Oysters in the short-term group underwent significant intracellular calcium variation and oxidative stress. In contrast, the intracellular calcium, ROS level in hemocytes and H₂O₂ in serum recovered to normal levels after long-term CO₂ exposure, suggesting the compensation of physiological status and mutual interplay between calcium and oxidative level. The compensation was supported by the up-regulation of a series of calcium binding proteins (CBPs) and calmodulins (CaMs) related signal pathway. The results provided valuable information to understand the molecular mechanism underlying the responses of Pacific oyster to the acidified ocean and might have implications for predicting the possible effects of global climate changes on oyster aquaculture.
Identification and molecular characterization of nitric oxide synthase (NOS) gene in the intertidal copepod Tigriopus japonicus
2016, Gene
Citation Excerpt :
The insect NOS system and its rapid inducibility in response to many different pathogens have been extensively studied (Nappi et al., 2000; Rivero, 2006; Davies, 2000; Marmaras and Lampropoulou, 2009; Park et al., 2013). NOS is also a pivotal component of the innate immune system and a cellular signal of environmental stress in aquatic invertebrates (Giovine et al., 2001; Palumbo, 2005). Particularly in aquatic crustaceans, LPS-triggered inducibility of NOS activity and NOS transcript level have been highlighted in the haemocyte tissues that play a crucial role in the innate immunity of invertebrates (Rodríguez-Ramos et al., 2010, 2011; Yao et al., 2010; Li et al., 2012; Jiang et al., 2013).
In copepods, no information has been reported on the structure or molecular characterization of the nitric oxide synthase (NOS) gene. In the intertidal copepod Tigriopus japonicus, we identified a NOS gene that is involved in immune responses of vertebrates and invertebrates. In silico analyses revealed that nitric oxide (NO) synthase domains, such as the oxygenase and reductase domains, are highly conserved in the T. japonicus NOS gene. The T. japonicus NOS gene was highly transcribed in the nauplii stages, implying that it plays a role in protecting the host during the early developmental stages. To examine the involvement of the T. japonicus NOS gene in the innate immune response, the copepods were exposed to lipopolysaccharide (LPS) and two Vibrio sp. After exposure to different concentrations of LPS and Vibrio sp., T. japonicus NOS transcription was significantly increased over time in a dose-dependent manner, and the NO/nitrite concentration increased as well. Taken together, our findings suggest that T. japonicus NOS transcription is induced in response to an immune challenge as part of the conserved innate immunity.
Immunotoxicity of washing soda in a freshwater sponge of India
2015, Ecotoxicology and Environmental Safety
Citation Excerpt :
Initial increase in the generation of superoxide anion and its subsequent decrease was indicative to a typical stress response of sponge cells under the exposure of sodium carbonate. Nitric oxide is considered as a signaling molecule generated in sponge cells during the conversion of l-arginine to l-citrulline, by nitric oxide synthase (Giovine et al., 2001). Nitric oxide plays a significant role in generating cytotoxic response against engulfed pathogens.
The natural habitat of sponge, Eunapius carteri faces an ecotoxicological threat of contamination by washing soda, a common household cleaning agent of India. Washing soda is chemically known as sodium carbonate and is reported to be toxic to aquatic organisms. Domestic effluent, drain water and various human activities in ponds and lakes have been identified as the major routes of washing soda contamination of water. Phagocytosis and generation of cytotoxic molecules are important immunological responses offered by the cells of sponges against environmental toxins and pathogens. Present study involves estimation of phagocytic response and generation of cytotoxic molecules like superoxide anion, nitric oxide and phenoloxidase in E. carteri under the environmentally realistic concentrations of washing soda. Sodium carbonate exposure resulted in a significant decrease in the phagocytic response of sponge cells under 4, 8, 16 mg/l of the toxin for 96 h and all experimental concentrations of the toxin for 192 h. Washing soda exposure yielded an initial increase in the generation of the superoxide anion and nitric oxide followed by a significant decrease in generation of these cytotoxic agents. Sponge cell generated a high degree of phenoloxidase activity under the experimental exposure of 2, 4, 8, 16 mg/l of sodium carbonate for 96 and 192 h. Washing soda induced alteration of phagocytic and cytotoxic responses of E. carteri was indicative to an undesirable shift in their immune status leading to the possible crises of survival and propagation of sponges in their natural habitat.
Stress response to cadmium and manganese in Paracentrotus lividus developing embryos is mediated by nitric oxide
2014, Aquatic Toxicology
Citation Excerpt :
The involvement of NO in the stress response has also been reported in other organisms. Heat stress activated NO production in sponges (Giovine et al., 2001), and salinity and light stress gave rise to NO bursts in culture media of marine microalgae (Zhang et al., 2006). NO was also a central player in the surveillance system in a marine diatom in response to decadienal treatment (Vardi et al., 2006) and in coral bleaching (Bouchard and Yamasaki, 2008).
Increasing concentrations of contaminants, often resulting from anthropogenic activities, have been reported to occur in the marine environment and affect marine organisms. Among these, the metal ions cadmium and manganese have been shown to induce developmental delay and abnormalities, mainly reflecting skeleton elongation perturbation, in the sea urchin Paracentrotus lividus, an established model for toxicological studies. Here, we provide evidence that the physiological messenger nitric oxide (NO), formed by l-arginine oxidation by NO synthase (NOS), mediates the stress response induced by cadmium and manganese in sea urchins. When NO levels were lowered by inhibiting NOS, the proportion of abnormal plutei increased. Quantitative expression of a panel of 19 genes involved in stress response, skeletogenesis, detoxification and multidrug efflux processes was followed at different developmental stages and under different conditions: metals alone, metals in the presence of NOS inhibitor, NO donor and NOS inhibitor alone. These data allowed the identification of different classes of genes whose metal-induced transcriptional expression was directly or indirectly mediated by NO. These results open new perspectives on the role of NO as a sensor of different stress agents in sea urchin developing embryos.

View all citing articles on Scopus

¹: To whom correspondence should be adressed. Fax: 00390103538116. E-mail: [email protected].

View full text

Regular ArticleHeat Stress-Activated, Calcium-Dependent Nitric Oxide Synthase in Sponges

Abstract

J. Auton. Nerv. Syst.

Vision Res.

Anal. Biochem.

Biochim. Biophys. Acta

Neurosci. Lett.

Nitric oxide: A physiologic messenger molecule

Annu. Rev. Biochem.

Nitric oxide synthases: Which, where, how, and why?

J. Clin. Invest.

Regular Article
Heat Stress-Activated, Calcium-Dependent Nitric Oxide Synthase in Sponges