A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Abstract

Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever.

Keywords: Dysbiosis; Ecosystem services; Evolution; Host-microbiota interactions; Marine holobionts; Symbiosis.

Figure 1. Partners forming marine holobionts.

They are widespread across the tree of life including all kingdoms (eukaryotes, bacteria, archaea, viruses), and represent a large diversity of potential models for exploring complex biotic interactions across lineages. Plain lines correspond to holobionts referred to in the present manuscript. Dashed lines are examples of potential interactions. Photo credits: Archaeplastida –Catherine Leblanc, Ulisse Cardini; Excavata - Roscoff Culture Collection (http://roscoff-culture-collection.org/rcc-strain-details/1065), Attribution 4.0 International (CC BY 4.0); Amoebozoa - Roscoff Culture Collection (http://roscoff-culture-collection.org/rcc-strain-details/1067), Attribution 4.0 International (CC BY 4.0); Cryptophyta –Roscoff Culture Collection (http://roscoff-culture-collection.org/rcc-strain-details/1998), Attribution 4.0 International (CC BY 4.0); Stramenopila –Catherine Leblanc, Simon M Dittami;Alveolata –Allison Lewis (https://commons.wikimedia.org/wiki/File:Symbiodinium.png), Creative Commons Attribution-Share Alike 4.0 International license; Rhizaria –Fabrice Not; Haptophyta –Alison R. Taylor (https://en.wikipedia.org/wiki/Emiliania_huxleyi#/media/Datei:Emiliania_huxleyi_coccolithophore_(PLoS).png), Attribution 2.5 Generic (CC BY 2.5); Opisthonkonta –HeikeM (https://fr.wikipedia.org/wiki/R%C3%A9cif_corallien_d%27eau_froide#/media/Fichier:Joon1.jpg, Public Domain), NOAA Photo Library (https://en.wikipedia.org/wiki/Sea_anemone#/media/File:Actinoscyphia_aurelia_1.jpg, Public Domain), Squid (Chris Frazee, Margaret McFall-Ngai, https://en.wikipedia.org/wiki/Squid#/media/File:Euprymna_scolopes_-_image.pbio.v12.i02.g001.png, Attribution 4.0 International (CC BY 4.0)); Bacteria –Marinobacter (Astrid Gärdes, Eva Kaeppel, Aamir Shehzad, Shalin Seebah, Hanno Teeling, Pablo Yarza, Frank Oliver Glöckner, Hans-Peter Grossart, Matthias S. Ullrich, https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3035377/figure/f1/, Attribution 2.5 Generic (CC BY 2.5)), Synecococcus (Masur, https://en.wikipedia.org/wiki/Synechococcus#/media/Datei:Synechococcus_PCC_7002_BF.jpg, Public Domain), Vibrio fischeri (Alan Cann, https://www.flickr.com/photos/ajc1/252308050/, Attribution-NonCommercial 2.0 Generic (CC BY-NC 2.0)), Hyphomonas - Holomarine consortium (Simon M Dittami);Archaea –Halobacterium (NASA, https://commons.wikimedia.org/wiki/File:Halobacteria.jpg, Public Domain), Sulfolobus (Xiangyux, https://de.wikipedia.org/wiki/Archaeen#/media/Datei:RT8-4.jpg, Public Domain);Viruses –Matthew B Sullivan, Maureen L Coleman, Peter Weigele, Forest Rohwer, Sallie W Chisholm (https://en.wikipedia.org/wiki/Cyanophage#/media/File:Cyanophages.png), Attribution 2.5 Generic (CC BY 2.5).

Figure 2. Schematic view of the “Russian Doll” complexity and dynamics of holobionts, according to diverse spatiotemporal scales.

The host (blue circles), and associated microbes (all other shapes) including bacteria and eukaryotes that may be inside (i.e., endosymbiotic) or outside the host (i.e., ectosymbiotic) are connected by either beneficial (solid orange lines), neutral (solid blue lines) or pathogenic (dashed black lines) interactions, respectively. Changes from beneficial or neutral to pathogenic interactions are typical cases of dysbiosis. The different clusters can be illustrated by the following examples: 1, a model holobiont in a stable physiological condition (e.g., in controlled laboratory condition); 2 and 3, holobionts changing during their life cycle or subjected to stress conditions—examples of vertically transmitted microbes are indicated by light blue arrows; 4 and 5, marine holobionts in the context of global sampling campaigns or long-term time series—examples of horizontal transmission of microbes and holobionts are illustrated by pink arrows.

Figure 3. Mind map of key concepts, techniques, and challenges related to marine holobionts.

The basis of this map was generated during the Holomarine workshop held in Roscoff in 2018 (https://www.euromarinenetwork.eu/activities/HoloMarine). The size of the nodes reflects the number of votes each keyword received from the participants of the workshop (total of 120 votes from 30 participants). The two main clusters corresponding to predictive modeling and mechanistic modeling, are displayed in purple and turquoise, respectively. Among the intermediate nodes linking these disciplines (blue) “potential use, management” was the most connected.

Figure 4. Impact of emerging methodologies (light green) on the main challenges in marine holobiont research identified in this paper (blue).

Turquoise and purple correspond to the two main clusters of activity identified in Fig. 3.