Sponge–Microbe Interactions on Coral Reefs: Multiple Evolutionary Solutions to a Complex Environment

Abstract

Marine sponges have been successful in their expansion across diverse ecological niches around the globe. Pioneering work attributed this success to both a well-developed aquiferous system that allowed for efficient filter feeding on suspended organic matter and the presence of microbial symbionts that can supplement host heterotrophic feeding with photosynthate or dissolved organic carbon. We now know that sponge-microbe interactions are host-specific, highly nuanced, and provide diverse nutritional benefits to the host sponge. Despite these advances in the field, many current hypotheses pertaining to the evolution of these interactions are overly generalized; these over-simplifications limit our understanding of the evolutionary processes shaping these symbioses and how they contribute to the ecological success of sponges on modern coral reefs. To highlight the current state of knowledge in this field, we start with seminal papers and review how contemporary work using higher resolution techniques has both complemented and challenged their early hypotheses. We outline different schools of thought by discussing evidence of symbiont contribution to both host ecological divergence and convergence, nutritional specificity and plasticity, and allopatric and sympatric speciation. Based on this synthesis, we conclude that the evolutionary pressures shaping these interactions are complex, with influences from both external (nutrient limitation and competition) and internal (fitness trade-offs and evolutionary constraints) factors. We outline recent controversies pertaining to these evolutionary pressures and place our current understanding of these interactions into a broader ecological and evolutionary framework. Finally, we propose areas for future research that we believe will lead to important new developments in the field.

Stability of the Microbiome of the Sponge Mycale (Oxymycale) acerata in the Western Antarctic Peninsula

“…The impacts of environmental factors on sponge–microbe relationships have been addressed by several studies carried out at different latitudes, with some studies assessing the effects at different ambient, temporal, and/or geographic scales ( Anderson et al, 2010 ; Erwin et al, 2012 , 2015 ; Luter et al, 2015 ; Easson et al, 2020 ), while others tested environmental stress obtaining variable results depending on the species and also on the duration and strength of the environmental alterations ( Webster et al, 2008 ; Fan et al, 2013 ; Cárdenas et al, 2014 ; Pineda et al, 2017 ; Ramsby et al, 2018 ). Previous studies have suggested the existence of strong interactions between geographic, environmental, and host factors influencing the microbiome of some species ( Easson et al, 2020 ; Freeman et al, 2021 ). Taking into account current environmental changes occurring around the globe, it is important to better understand the sponge–microbiota patterns in terms of temporal and spatial scales as well as intra- and interspecific variations and its key ecosystem functions in order to better understand and predict potential direct and cascading effects produced by future environmental changes.…”

Investigation of Global Trends of Pollutants in Marine Ecosystems around Barrang Caddi Island, Spermonde Archipelago Cluster: An Ecological Approach

“…In terms of types of low-toxic PAH, the NL type was identified in all samples. NL is a simple aromatic hydrocarbon [9,38,116]. Naphthalene-based products, such as camphor, are thought to come from household activities, for example, in products used to eradicate insects and absorb odors in bathroom toilets.…”

“…The presence of PR in the sample is thought to have come from the transportation activities of petroleum carriers. This assumption was reinforced by the identification of the PAH type AZ, as the PAH type is a component of petroleum as are some of its derivative products, including those from coal processing [9,84,118]. This allegation is quite reasonable, because BCI operates three ports: a container port, a passenger port, and a fish-landing port.…”

“…The abundance of PAH components in the samples occurred in the following order: NL >> BZ >AZ >PR >PH. The peak numbers in the recorded GS/MS chromatograms are sequential, according to the number of components [9,74]. However, some peak numbers are not included in the data (Table 1), indicating that the peak number is not considered to be a PAH component or that it may be a derivative of a type of PAH, but the level of similarity with the standard library on the instrument does not reach 85% [88,90,91].…”

“…Most human waste material can occur in all of the regions of the earth. Due to the influences of ecology and gravity, garbage has the potential to end up in the sea, either intentionally or due to negligence in managing the marine environment [9][10][11].…”