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1.
ISME J ; 16(9): 2076-2086, 2022 09.
Article in English | MEDLINE | ID: mdl-35654830

ABSTRACT

The ability of organisms to combine autotrophy and heterotrophy gives rise to one of the most successful nutritional strategies on Earth: mixotrophy. Sponges are integral members of shallow-water ecosystems and many host photosynthetic symbionts, but studies on mixotrophic sponges have focused primarily on species residing in high-light environments. Here, we quantify the contribution of photoautotrophy to the respiratory demand and total carbon diet of the sponge Chondrilla caribensis, which hosts symbiotic cyanobacteria and lives in low-light environments. Although the sponge is net heterotrophic at 20 m water depth, photosynthetically fixed carbon potentially provides up to 52% of the holobiont's respiratory demand. When considering the total mixotrophic diet, photoautotrophy contributed an estimated 7% to total daily carbon uptake. Visualization of inorganic 13C- and 15N-incorporation using nanoscale secondary ion mass spectrometry (NanoSIMS) at the single-cell level confirmed that a portion of nutrients assimilated by the prokaryotic community was translocated to host cells. Photoautotrophy can thus provide an important supplemental source of carbon for sponges, even in low-light habitats. This trophic plasticity may represent a widespread strategy for net heterotrophic sponges hosting photosymbionts, enabling the host to buffer against periods of nutritional stress.


Subject(s)
Porifera , Solar Energy , Animals , Carbon , Diet , Ecosystem , Water
2.
Microbiome ; 9(1): 44, 2021 02 14.
Article in English | MEDLINE | ID: mdl-33583434

ABSTRACT

BACKGROUND: Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of 13C- and 15N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea. RESULTS: The two sponge species showed significant enrichment of DOM- and POM-derived 13C and 15N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome. CONCLUSIONS: Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan-microbe symbioses. Video abstract.


Subject(s)
Microbiota/physiology , Nutrients/metabolism , Porifera/metabolism , Porifera/microbiology , Symbiosis , Animals , Carbon/metabolism , Nitrogen/metabolism
3.
Dev Comp Immunol ; 48(2): 360-8, 2015 Feb.
Article in English | MEDLINE | ID: mdl-24796867

ABSTRACT

Future expansion of the crustacean aquaculture industry will be required to ensure global food security. However, this expansion must ensure: (a) that natural resources (including habitat use and fish meal) are sustainably exploited, (b) that the socio-economic development of producing nations is safeguarded, and (c) that the challenge presented by crustacean diseases is adequately met. Conventionally, the problem of disease in crustacean aquaculture has been addressed through prophylactic administration of stimulants, additives or probiotics. However, these approaches have been questioned both experimentally and philosophically. In this review, we argue that real progress in the field of crustacean immune stimulants has now slowed, with only incremental advances now being made. We further contend that an overt focus on the immune effector response has been misguided. In light of the wealth of new data reporting immune system complexity, a more refined approach is necessary - one that must consider the important role played by pattern recognition proteins. In support of this more refined approach, there is now a much greater requirement for the reporting of essential metadata. We propose a broad series of recommendations regarding the 'Minimum Information required to support a Stimulant Assessment experiment' (MISA guidelines) to foster new progression within the field.


Subject(s)
Aquaculture , Crustacea/immunology , Crustacea/microbiology , Shellfish/microbiology , Animals , Aquaculture/economics , Aquaculture/standards , Arthropod Proteins/immunology , Food Supply , Immune System , Receptors, Pattern Recognition/immunology
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