The sponge holobiont in a changing ocean: from microbes to ecosystems

Pita et al. Microbiome (2018) 6:46 https://doi.org/10.1186/s40168-018-0428-1 REVIEW Open Access The sponge holobiont in a changing ocean: from microbes to ecosystems L. Pita1*† , L. Rix1† , B. M. Slaby1 , A. Franke1 and U. Hentschel1,2 Abstract The recognition that all macroorganisms live in symbiotic association with microbial communities has opened up a new field in biology. Animals, plants, and algae are now considered holobionts, complex ecosystems consisting of the host, the microbiota, and the interactions among them. Accordingly, ecological concepts can be applied to understand the host-derived and microbial processes that govern the dynamics of the interactive networks within the holobiont. In marine systems, holobionts are further integrated into larger and more complex communities and ecosystems, a concept referred to as “nested ecosystems.” In this review, we discuss the concept of holobionts as dynamic ecosystems that interact at multiple scales and respond to environmental change. We focus on the symbiosis of sponges with their microbial communities—a symbiosis that has resulted in one of the most diverse and complex holobionts in the marine environment. In recent years, the field of sponge microbiology has remarkably advanced in terms of curated databases, standardized protocols, and information on the functions of the microbiota. Like a Russian doll, these microbial processes are translated into sponge holobiont functions that impact the surrounding ecosystem. For example, the sponge-associated microbial metabolisms, fueled by the high filtering capacity of the sponge host, substantially affect the biogeochemical cycling of key nutrients like carbon, nitrogen, and phosphorous. Since sponge holobionts are increasingly threatened by anthropogenic stressors that jeopardize the stability of the holobiont ecosystem, we discuss the link between environmental perturbations, dysbiosis, and sponge diseases. Experimental studies suggest that the microbial community composition is tightly linked to holobiont health, but whether dysbiosis is a cause or a consequence of holobiont collapse remains unresolved. Moreover, the potential role of the microbiome in mediating the capacity for holobionts to acclimate and adapt to environmental change is unknown. Future studies should aim to identify the mechanisms underlying holobiont dynamics at multiple scales, from the microbiome to the ecosystem, and develop management strategies to preserve the key functions provided by the sponge holobiont in our present and future oceans. Keywords: Sponges, Holobiont, Health, Symbiosis, Microbiome, Nested ecosystems, Stress, Climate change, Dysbiosis, Disease Background Marine animals live and evolve in a sea of microbes. The ocean is the largest habitat on our planet and microbes are its most abundant inhabitants. These microorganisms (i.e., viruses, bacteria, archaea, microeukaryotes) play a key role in global biogeochemical cycles [1]; yet, scientists are only beginning to reveal their genomic and metabolic diversity [2]. Marine microbes exist not only in a planktonic state but also in symbiosis with * Correspondence: † Equal contributors 1 RD3 Marine Microbiology, GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germany Full list of author information is available at the end of the article macroorganisms: animals, plants, and algae alike [3, 4]. The prevalence of these associations implies that multicellular organisms can no longer be considered as autonomous entities [5] but rather as holobionts (syn. “metaorganisms” [6]), encompassing the host plus its associated microbiota [7, 8]. The microbial partners contribute to the nutrition [9], defense [10], immunity [11], and development [12] of the host; thereby collectively influencing its health and functioning. The first approaches to define the holobiont consisted of characterizing the set of microbial taxa common to all individuals of a certain species, the core microbiota. Later definitions, enabled by massively increased © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Pita et al. Microbiome (2018) 6:46 Box 1 Glossary Acclimatization: The capacity of a holobiont to adjust to a perturbation through host phenotypic plasticity or restructuring of the microbiome in order to reach a new stable state Adaptation: A transgenerational process that enhances the fitness of the holobiont through transgenerational acclimatization, heritable microbial community changes, or host/symbiont evolution Core microbiome: The set of microbial taxa which are consistently and stably prevalent in host individuals of the same species Dysbiosis: The divergence of a symbiotic microbial community from the community found in healthy individuals Disease: The impairment of normal function following perturbation or damage. May be, but is not necessarily, induced by a pathogenic microorganism Functional convergence: In the holobiont context, symbiotic microbial communities with different evolutionary histories that have, via different but analogous pathways, converged upon similar functional solutions Functional redundancy: The presence of several microbial taxa within an ecosystem or holobiont that perform the same functions, such that the loss of one particular taxon or a shift in the community diversity would not compromise ecosystem function Holobiont health: A dynamic equilibrium that allows minor fluctuations in terms of diversity or functions to ensure the maintenance of symbiotic homeostasis Microbiota: The assemblage of microorganisms present in a defined environment or host Microbiome: The group of microbes, their genetic information, and the surrounding environmental conditions in a defined environment or host Nested ecosystem: A smaller distinct ecosystem which is contained within and interacts with a larger ecosystem or series of successively larger ecosystems Opportunistic: An organism that is capable of causing damage to a host under specific conditions, but may also exist as a commensal within the same host under normal conditions Perturbation: A temporary or persistent change in biotic or abiotic conditions that leads to a response by an ecosystem or holobiont Resilience: The capacity of a system to recover its initial functional and taxonomical composition and return to an initial stable state following a perturbation Resistance: The property of a system to remain unchanged and mainta (...truncated)