1- Introduction

2- Materials and methods

3- Results

4- Discussion

References

Abstract

Photosynthesis is an important driver of calcium carbonate deposition on tropical coral reefs largely due to the symbiosis of numerous invertebrates with photosynthetic dinoflagellates in the family Symbiodiniaceae. In bioeroding sponges, however, similar symbioses appear to support the decalcification of carbonate substrates. Compared to its role in calcification, the relative importance of photosynthesis to decalcification processes is less known. Here, the daytime and night-time chemical bioerosion rates of the common Indo-Pacific sponge Cliona orientalis were examined under varying levels of photosynthetic activity and/or varying abundances of intracellular dinoflagellates. Photosynthesis was manipulated either by preconditioning the sponges with the photosynthetic inhibitor diuron (DCMU), or by exposing them to short-term heat stress to achieve bleaching (loss of symbionts). DCMU reduced symbiont numbers and diminished their ability to evolve oxygen. Thermal stress caused a significantly greater loss of symbionts, but photosynthesis was less inhibited. In both cases, decreases in photosynthetic activity and symbiont densities led to proportionately lowered daytime chemical bioerosion rates. Moreover, increased rates of night-time bioerosion were linked to greater daytime rates of photosynthesis, rather than to the night-time respiration of the sponge holobiont. Our findings support the conclusion that photosynthetic products (photosynthates) and/or by-products (oxygen) stimulate sponge bioerosion. This work further reveals the importance of symbionts in the ecology of such sponges and in their ability to sustain high bioerosion activity in otherwise nutrient-poor ecosystems.

Introduction

Tropical coral reefs thrive in shallow clear waters where sunlight powers productive and diverse food chains. Symbioses between invertebrates and a variety of photosynthetic microorganisms enable high rates of productivity on reefs despite low environmental concentrations of inorganic nutrients (Muscatine and Porter, 1977; Seckbach, 2004; Yellowlees et al., 2008). The evolutionary success that results from hosting phototrophic microbes such as dinoflagellates, diatoms, chlorophytes, rhodophytes, or cyanobacteria is seen in a wide range of diverse invertebrates belonging to taxa such as Cnidaria, Mollusca, Foraminifera, Platyhelminthes, and Porifera (Trench, 1993; Stat et al., 2006; Lipps and Stanley, 2016). Presently almost 200 sponge species (Porifera) are known to host microbial photosynthetic symbionts (“photosymbiotic” sponges), which may contribute to the nutrition and health of the sponge (e.g. Wilkinson, 1987; Hill et al., 2011; Thacker and Freeman, 2012). Sponge species that receive substantial contributions in this way are often named “phototrophic” after the nutritional mode of their symbionts, or “mixotrophic” given that they also depend on filter-feeding by specialized food-trapping sponge cells. The nutrition of sponges is often further supplemented by inputs from intimate associations formed with heterotrophic bacterial populations of varying density and diversity (e.g. Hentschel et al., 2003; Taylor et al., 2007).

Despite a considerable amount of research to find alternatives to heavy metals (commonly defined as metals both heavier than 5 g/cm3 and toxic at low concentrations) (Ricco et al. 2015), they still find ever increasing usage in modern products, including batteries, pesticides, paints, and electronics. Consequently, the rising presence of heavy metal waste in the environment provides a potential and possibly increasing risk of prolonged health problems to humans and other living species. For example, lead poisoning can severely affect central nervous systems (Okoye et al. 2010); cadmium compounds are likely human carcinogens, longterm exposure may cause fragile bones, kidney damage, and even death (Boparai et al. 2011; Srivastava et al. 2006); symptoms of copper poisoning include nausea, vomiting, and death (Fu and Wang 2011). These problems are exacerbated by the fact that heavy metals are usually not easily removed from the biosphere but instead tend to accumulate in living organisms (Annadurai et al. 2003; Fu and Wang 2011; Reed and Matsumoto 1993), making the problem of heavy metal contamination more severe. Therefore, simple and effective treatments for water contaminated with heavy metals have received continuous attention (Fu and Wang 2011). Existing methods for heavy metal removal from water include chemical precipitation (Charerntanyarak 1999; Matlock et al. 2002), ion exchange (Tavakoli et al. 2017; Wang et al. 2014), membrane filtration (Al-Rashdi et al. 2013; Blöcher et al. 2003), and adsorption (Celis et al. 2000; Ho et al. 1996). Among these technologies, adsorption is one of the most promising methods, as it is generally passive and relatively facile. Recently, several types of adsorbents have been reported for removing heavy metals from water, including carbon nanotubes (Stafiej and Pyrzynska 2007), activated carbon (Amuda et al. 2007; Kobya et al. 2005), zeolites (Erdem et al. 2004), metal-organic frameworks (MOFs) (Ricco et al. 2015), nanosized metal oxides (Hua et al. 2012; Wang et al. 2010a), and resins (Lin et al. 2000). Among these adsorbents (Table 1), nano-adsorbents such as carbon nanotubes, MOFs, or metal oxide nanomaterials show a high capacity for adsorbing metal ions from aqueous solution due to their high surface areas; however, these adsorbents can be expensive and difficult to prepare (Gupta et al. 2011). Therefore, there is a pressing need for adsorbents that are cost-effective, abundant, easy to prepare, biocompatible, and capable of efficiently removing heavy metals, that is, absorption that is fast and extensive.

Periapical lesion results from serious inflammatory response to microorganisms around the tooth root and the root canal [1]. Periapical lesions could perforate into the oral cavity affecting hard tissue or maxillary sinus. The infection around the root and tooth leads to bone resorption caused by local osteomyelitis [2]. Furthermore, cellulitis in soft tissue causing swelling in the face is a common symptom of severe local jawbone osteomyelitis. Traumatic injuries of teeth can cause granuloma or cysts associated with periapical lesions. Granulomas are composed usually of solid soft tissue, while cysts are semisolid tissue surrounded by epithelium [3]. Radiographs show lesions structure as unilocular, lucent, round, or pear shaped contoured by a thin rim of cortical bone [4]. The incidence of cysts formation is between 6 and 55% in small lesions and a 100% with lesions larger than 20 mm [2]. On the other hand, granulomas occurrence ranges between 9.3 and 87.1%, where abscesses formation rate is between 28.7 and 70.07% [4]. Epithelial proliferation and other molecular mechanisms can cause lesion formation. Nonetheless, by-products of microorganisms, which lead to osmotic fluid accumulation in the lumen, are the most common cause of periapical lesions [5]. Therefore, eliminating microorganisms can release the hydrostatic pressure resulting from osmotic fluid and minimize the effect of periapical lesions on the tooth. Management of infection-caused periapical lesions is a two-step process. Firstly, antibacterial treatment is performed using antibiotics (e.g., metronidazole, ciprofloxacin, and minocycline), chemical irrigation, and disinfectants (i.e., calcium hydroxide). Despite its wide use as disinfectant of the root canal system, calcium hydroxide is not effective as root canal dressing [2, 6, 7]. Secondly, releasing the hydrostatic pressure is detrimental and can be achieved by decompression, aspiration, and aspiration irrigation [8–10].