Release of dissolved and particulate organic matter by the soft coral Lobophytum and subsequent microbial degradation

Nakajima, Reiko; Haas, Andreas F.; Silveira, Cynthia B.; Kelly, Emily L. A.; Smith, Jennifer E.; Sandin, Stuart A.; Kelly, Linda Wegley; Rohwer, Forest; Nakatomi, Nobuyuki; Kurihara, Haruko

doi:10.1016/j.jembe.2018.02.008

Cited by 12 publications

(15 citation statements)

References 55 publications

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“…Finally, the organic matter (OM) released by soft corals presented a particularly low POC:PN ratio (of 5–7, i.e., particles enriched in N) compared to the OM released by scleractinian corals (from 12–17 in this study, range in agreement with Naumann et al, 2010). This is also in agreement with the findings of two previous studies (Meikle et al, 1988; Nakajima et al, 2018), which observed a higher protein and lower carbohydrate composition of soft coral mucus compared to scleractinian coral mucus. Since N 2 fixation is rather promoted by N deprivation (Knapp, 2012), a low POC:PN ratio is not in favor of N 2 fixation.…”

Section: Discussionsupporting

confidence: 93%

“…This is in agreement with previous measurements performed on another Red Sea soft coral belonging to the Xeniidae family, for which no POC release was observed (Bednarz et al, 2012). As POC is a proxy for detrital and living particles, the lower particle content in the soft coral surrounding seawater can be explained by the well-known antimicrobial properties of soft coral mucus (Kelman et al, 2006; Nakajima et al, 2018). These authors indeed demonstrated that little antimicrobial activity was measured for scleractinian coral mucus whereas soft corals, including those studied in this work, significantly inhibited the growth of co-occurring seawater bacteria through the production of antibiotic compounds.…”

Section: Discussionmentioning

confidence: 99%

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Divergent Capacity of Scleractinian and Soft Corals to Assimilate and Transfer Diazotrophically Derived Nitrogen to the Reef Environment

et al. 2019

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Corals are associated with dinitrogen (N 2 )-fixing bacteria that potentially represent an additional nitrogen (N) source for the coral holobiont in oligotrophic reef environments. Nevertheless, the few studies investigating the assimilation of diazotrophically derived nitrogen (DDN) by tropical corals are limited to a single scleractinian species (i.e., Stylophora pistillata ). The present study quantified DDN assimilation rates in four scleractinian and three soft coral species from the shallow waters of the oligotrophic Northern Red Sea using the 15 N 2 tracer technique. All scleractinian species significantly stimulated N 2 fixation in the coral-surrounding seawater (and mucus) and assimilated DDN into their tissue. Interestingly, N 2 fixation was not detected in the tissue and surrounding seawater of soft corals, despite the fact that soft corals were able to take up DDN from a culture of free-living diazotrophs. Soft coral mucus likely represents an unfavorable habitat for the colonization and activity of diazotrophs as it contains a low amount of particulate organic matter, with a relatively high N content, compared to the mucus of scleractinian corals. In addition, it is known to present antimicrobial properties. Overall, this study suggests that DDN assimilation into coral tissues depends on the presence of active diazotrophs in the coral’s mucus layer and/or surrounding seawater. Since N is often a limiting nutrient for primary productivity in oligotrophic reef waters, the divergent capacity of scleractinian and soft corals to promote N 2 fixation may have implications for N availability and reef biogeochemistry in scleractinian versus soft coral-dominated reefs.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Divergent Capacity of Scleractinian and Soft Corals to Assimilate and Transfer Diazotrophically Derived Nitrogen to the Reef Environment

et al. 2019

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“…Bacterial stimulation and SSW in asteroids is paralleled by the DDAM (dissolved organic carbon, disease, algae, microorganism) positive feedback loop in tropical corals ( Dinsdale et al, 2008 ; Barott and Rohwer, 2012 ; Silveira et al, 2019 ). Coral disease is associated with OM cenrichment ( Kline et al, 2006 ; Smith et al, 2006 ), some of which originates from sympatric primary producers ( Haas et al, 2010 , 2011 ), which in turn are more labile than OM released from the corals themselves ( Haas et al, 2016 ; Nakajima et al, 2018 ) and results in both elevated bacterial abundance on coral surfaces ( Dinsdale and Rohwer, 2011 ; Haas et al, 2016 ), and enhanced remineralization rates ( Haas et al, 2016 ). In black band disease, DOC released from primary production causes micro-zones of hypoxia which result in production of toxic sulfides, which in turn result in opening of niches for cyanobacteria ( Sato et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease

et al. 2021

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Sea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of SSW is unresolved. We hypothesized that SSW is a sequela of microbial organic matter remineralization near respiratory surfaces, one consequence of which may be limited O2 availability at the animal-water interface. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before SSW onset, followed by the appearance of putatively facultative and strictly anaerobic taxa at the time of lesion genesis and as animals died. SSW lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources. These results together illustrate that depleted O2 conditions at the animal-water interface may be established by heterotrophic microbial activity in response to organic matter loading. SSW was also induced by modestly (∼39%) depleted O2 conditions in aquaria, suggesting that small perturbations in dissolved O2 may exacerbate the condition. SSW susceptibility between species was significantly and positively correlated with surface rugosity, a key determinant of diffusive boundary layer thickness. Tissues of SSW-affected individuals collected in 2013–2014 bore δ15N signatures reflecting anaerobic processes, which suggests that this phenomenon may have affected asteroids during mass mortality at the time. The impacts of enhanced microbial activity and subsequent O2 diffusion limitation may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential.

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“…Bacterial stimulation and enhanced wasting in asteroids is paralleled by the DDAM (dissolved organic carbon, disease, algae, microorganism) positive feedback loop in tropical corals (Dinsdale et al, 2008;Barott and Rohwer, 2012;Silveira et al, 2019). Coral disease is associated with OM enrichment (David et al, 2006;Smith et al, 2006), some of which originates from sympatric primary producers (Haas et al, 2010;Haas et al, 2011), which in turn are more labile than OM released from the corals themselves (Haas et al, 2016;Nakajima et al, 2018) and results in both elevated bacterial abundance on coral surfaces (Dinsdale and Rohwer, 2011;Haas et al, 2016), and enhanced remineralization rates (Haas et al, 2016). Bacteria at the coral-water interface have higher energetic demands than those in plankton (Roach et al, 2017), and are highly adapted to organic carbon availability in their local environment (Kelly et al, 2014).…”

Section: Shifts In Heterotrophic Bacterial and Archaeal Communities Dmentioning

confidence: 99%

Evidence that non-pathogenic microorganisms drive sea star wasting disease through boundary layer oxygen diffusion limitation

Aquino

Besemer

DeRito

et al. 2020

Preprint

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Sea star wasting (SSW) disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of sea star wasting is unresolved. We hypothesize that asteroid wasting is a sequela of microbial organic matter remineralization near respiratory surfaces which leads to boundary layer oxygen diffusion limitation (BLODL). Wasting lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before wasting onset, concomitant with and followed by the proliferation of putatively facultative and strictly anaerobic taxa. Bacterial cell abundance increased dramatically prior to wasting onset in experimental incubations. Wasting susceptibility was significantly correlated with rugosity (a key determinant of boundary layer thickness) of animal surfaces. At a semi continuously monitored field site (Langley Harbor), wasting predictably occurred at annual peak or decline in phytoplankton biomass. Finally, wasting individuals from 2013 to 2014 bore stable isotopic signatures reflecting anaerobic processes and altered C and N metabolisms. These convergent lines of evidence support our hypothesis that BLODL is associated with wasting both in contemporary SSW events and during the 2013 to 2014 SSW mass mortality event, potentially driven by phytoplankton-derived OM. The impacts of BLODL may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential.

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Release of dissolved and particulate organic matter by the soft coral Lobophytum and subsequent microbial degradation

Cited by 12 publications

References 55 publications

Divergent Capacity of Scleractinian and Soft Corals to Assimilate and Transfer Diazotrophically Derived Nitrogen to the Reef Environment

Divergent Capacity of Scleractinian and Soft Corals to Assimilate and Transfer Diazotrophically Derived Nitrogen to the Reef Environment

Evidence That Microorganisms at the Animal-Water Interface Drive Sea Star Wasting Disease

Evidence that non-pathogenic microorganisms drive sea star wasting disease through boundary layer oxygen diffusion limitation

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