Metabolic responses of a phototrophic sponge to sedimentation supports transitions to sponge-dominated reefs

Abstract

Declines in coral abundance have been linked to increased sedimentation at many locations across the world and at some of these locations there have been subsequent increases in sponge abundance. These shifts appear counterintuitive as sponges are suspension feeders and many rely on photosymbionts for carbon. At a sedimented reef in Indonesia (Wakatobi) corals have declined and the photoautotrophic sponge Lamellodysidea herbacea is now abundant. We hypothesise that this is partly due to L. herbacea’s ability to clear its tissues of high levels of settled-sediment and compensate for associated metabolic demands by altering its respiration rate. Negligible detrimental effects to sponge tissue were observed after treatments up to five times the sedimentation rate of the highly sedimented reef. Rapid sediment clearance occurred that was potentially aided by mucus production. Finally, high sediment exposure caused an immediate reduction in respiration rate, likely due to reduced pumping to prevent clogging, whereas sustained high sedimentation caused an increase in respiration rate, potentially due to the energetic cost of mucus production. Our study provides evidence that some sponges can tolerate environments that appear unsuitable to many corals and with increased sedimentation this acclimation may support further transitions to sponge dominated reefs in the future.

A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes

“…These hypotheses are supported by results in the current study, where multiple samples from Lamellodysidea herbacea sponges, noted for high seawater pumping rates[3], contain a predominance of bacteria favoring aerobic rather than anaerobic metabolic pathways, with low overall community diversity.The Lamellodysidea herbacea sponge microbiome has previously been characterized almost exclusively in terms of functional activities associated with its most dominant symbiont, Hormoscilla spongeliae. The results of this study reveal previously unreported potential metabolic activities, interactions, and community contributions of non-Hormoscilla species.…”

“…The prodigious seawater pumping capabilities of filter-feeding marine sponges contribute significantly to carbon cycling in global reef habitats, through the breakdown and remineralization of both dissolved and particulate forms of organic matter [1][2][3]. Nutrient recycling is facilitated by hostassociated microbial communities comprised of diverse sponge-specific taxa [4], including Gammaand Alphaproteobacteria, Acidobacteria, Actinobacteria, Chloroflexi, Cyanobacteria, Nitrospirae, Tectomicrobia, candidate phylum Poribacteria, and archaeal Thaumarchaeota (reviewed in [5,6]).…”

Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop

“…Sponge detritus is hypothesized to be largely due to high cell turnover and shedding, particularly of sponge choanocyte cells (de Goeij et al 2009, Alexander et al 2014. However, sponges may also release detritus by ejecting waste products and incompletely digested food (Maldonado 2016) or via other mechanisms such as mucus production in response to sedimentation (Bell et al 2015, Biggerstaff et al 2017. Sponge cell turnover and shedding is reduced under suboptimal food conditions (Alexander et al 2015b) and in wounded sponges (Alexander et al 2015a), suggesting a complex interplay of factors such as food availability, predation, reproductive status, growth rate and sponge health may govern detritus production.…”

Sedimentation limits the erosion rate of a bioeroding sponge

“…Mucus threads are also often observed on the surface of sedimented S. cf. vagabunda, which in other species are thought to aid sediment clearance (Biggerstaff, Smith, Jompa, & Bell, 2017). Active sediment clearance mechanisms such as morphological changes and mucus production can have a high metabolic cost (Bannister, Battershill, & De Nys, 2012;Biggerstaff et al, 2017) and could mean the diversion of energy away from other activities such as bioerosion.…”

“…vagabunda, which in other species are thought to aid sediment clearance (Biggerstaff, Smith, Jompa, & Bell, 2017). Active sediment clearance mechanisms such as morphological changes and mucus production can have a high metabolic cost (Bannister, Battershill, & De Nys, 2012;Biggerstaff et al, 2017) and could mean the diversion of energy away from other activities such as bioerosion. Sedimentation can also cause a reduction in pumping activity, resulting in decreased nutritional uptake (Gerrodette & Flechsig, 1979;Tompkins-MacDonald & Leys, 2008).…”