Corals and Sponges Under the Light of the Holobiont Concept: How Microbiomes Underpin Our Understanding of Marine Ecosystems

Abstract

In the past 20 years, a new concept has slowly emerged and expanded to various domains of marine biology research: the holobiont. A holobiont describes the consortium formed by a eukaryotic host and its associated microorganisms including bacteria, archaea, protists, microalgae, fungi, and viruses. From coral reefs to the deep-sea, symbiotic relationships and host–microbiome interactions are omnipresent and central to the health of marine ecosystems. Studying marine organisms under the light of the holobiont is a new paradigm that impacts many aspects of marine sciences. This approach is an innovative way of understanding the complex functioning of marine organisms, their evolution, their ecological roles within their ecosystems, and their adaptation to face environmental changes. This review offers a broad insight into key concepts of holobiont studies and into the current knowledge of marine model holobionts. Firstly, the history of the holobiont concept and the expansion of its use from evolutionary sciences to other fields of marine biology will be discussed. Then, the ecology and physiology of marine holobionts will be investigated through the examples of corals and sponges. We will discuss the impacts of environmental change on organisms at the holobiont level and how microbiomes contribute to the resilience and/or vulnerability of their host in the face of environmental stressors. Finally, we will conclude with the development of new technologies, holistic approaches, and future prospects for conservation biology surrounding marine holobionts.

Volatile Organic Compounds, Indole, and Biogenic Amines Assessment in Two Mediterranean Irciniidae (Porifera, Demospongiae)

“…Since the fundamental role played by sponge symbionts is the synthesis of bioactive compounds [7,40], these results point out that differences exist in the microbiota colonizing Iv and Ss. Indeed, these species, like all the members of the family Irciniidae, are classified as high microbial abundance sponges, whose associated microorganisms can perform a wide range of functions of ecological interest.…”

Reconstitution and Transmission of Gut Microbiomes and Their Genes between Generations

“…In addition, Russell observed that a higher frequency of vertical transmission existed on land and a higher frequency of horizontal transmission existed in aquatic environments [226,227]. The observation of horizontal transmission being more abundant in the marine than in terrestrial environment could arise from the simple fact that water is a conducive medium in which desiccation and osmolarity do not represent a problem, thus encouraging horizontal transmission and host to-host transfer events [4]. For example, in the sponge, Plakina cyanorosea, harboring a relatively low microbial abundance, transmission of its microbiome relies primarily, but not exclusively, on horizontal transmission [220].…”

“…The microbiome genome is dynamic and changes more rapidly than the host genome. These principles stress the strong connection between the microbiome and the host in which a mutual adaptation has to evolve to achieve the robustness necessary for long-term survival [3,4]. Moreover, if these four principles are correct, then a holobiont with its hologenome is a level of selection in evolution [1,5].…”

“…It should be mentioned that several recent reviews have been published on different aspects of microbiome transmission. These reviews discuss plant microbiomes [12][13][14][15], animal microbiomes [4,[16][17][18][19][20], and human microbiomes [21][22][23][24][25]. This article is an updated opinion review that discusses plants and animals, including humans.…”

Assessing the coral microbiome at the scale of tissue-specific habitats within the coral meta-organism

“…Most studies investigating the coral microbiome have predominately focused on profiling microbial communities via next generation sequencing of 16S rRNA gene amplicons using whole fragments of individual corals, such as sections of branches collected from the colony of a branching coral species. Ultimately, the goal of these studies is to characterize coral-microbe interactions in different coral species (or morphotypes) in response to the combined challenges of environmental change (Stevenne et al, 2021). Considering the unique biotic interactions and dynamic relationships between the microbiome and the environment of morphologically, structurally, and functionally different coral hosts when assessing the response of the coral meta-organism may aid in meeting this goal.…”