Cellular Dialogues in the Holobiont

Thomas C. G. Bosch, Michael G. Hadfield

• Publisher: CRC Press
• Year: 2020
• ISBN:
  9781000090482
• Edition: 1
• Topic: Biological Sciences
• Subtopic: Biology
• Index: Biological Sciences

This book examines how the growing knowledge of the huge range of protist-, animal-, and plant-bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of biology. The establishment and maintenance of these interactions and their contributions to the health and survival of all partners relies on continuous cell-to-cell communication between them. This dialogue may be concerned with all aspects of the biology of both partners. The book includes chapters devoted to exploring, explaining, and exposing these dialogues across a broad spectrum of plant and animal eukaryotes to a broad field of biologists.

Key Features:

• Explores the nature of the interactions between eukaryotic hosts and their microbial symbionts
• Examines the links between prostist, animal, and plant evolution and microbial communities
• Reviews specific taxa and the microbial diversity associated with these taxa
• Illustrates the role microbes play in the physiology and etiology of several model species
• Includes chapters by an international team of leading scholars

The Open Access version of this book, available at http://www.taylorfrancis.com, has been made available under a Creative Commons Attribution-Non Commercial-No Derivatives (CC-BY-NC-ND) 4.0 license.

1

When does symbiosis begin? Bacterial cues necessary for metamorphosis in the marine polychaete Hydroides elegans

Marnie Freckelton and Brian T. Nedved

Contents

1.1 The symbiosis space

1.2 Chemical cues mediate symbiotic interactions

1.3 How do specific symbiotic interactions begin? Examples from the pre-symbiosis space

1.4 Bacterially induced metamorphosis of marine invertebrate animals

1.5 Bacterial induction of metamorphosis in Hydroides elegans

1.6 Identification of larval metamorphic cues from biofilm bacteria

1.7 How variability of inductive bacteria and identified settlement cues relate to variable larval settlement and recruitment

1.8 Lipopolysaccharide mediates both symbiotic and pre-symbiotic interactions

1.9 Conclusion

References

1.1 The symbiosis space

Symbiosis, the living together of unlike organisms (de Bary 1879), has become one of the most important concepts in biology today. This has been especially true since the discovery of the prevalence of microbiomes (Woese 2004; Moran and Dunbar 2006) and the role of the holobiont (Margulis 1971) in shaping both individual health and development, the evolution of biological complexity, and ecosystem-wide processes (Bordenstein and Theis 2015). It is through this cooperation of individuals that new habitats and energy sources can be accessed and utilized (Moran and Dunbar 2006; Fisher et al. 2017). In the marine environment, cooperative prokaryotic-eukaryotic interactions have drastically increased the rate at which organisms adapt to utilize new environments and energy sources (Apprill 2020).

Symbiosis, however, is not a discrete concept but rather extends across a spectrum of interactions defined by three axes: impact on host fitness (positive to negative), the dependency of the relationship, and the residency of the symbiotic relationship. In prokaryotic–eukaryotic symbioses, the evolutionary relationship is considered to start with complex, nonessential interactions, progress to facultative and then finally to obligate symbiotic relationships (Moya et al. 2008). At the terminus of this progression, we have obligate endosymbiotic relationships (mutualisms) where neither individual can survive independently, for instance, the pea aphid Acyrthosiphon pisum and its endosymbiont Buchnera aphidicola (Scarborough et al. 2005; Shigenobu and Wilson 2011), whereas legumes and rhizobial bacteria, a facultative commensalism, sit earlier in the continuum. Current models of symbiosis are heavily skewed towards the terminus of this evolutionary progression, obligate mutualistic endosymbiosis. However, many symbioses in the marine environment fall early in the continuum, and, while some of these relationships progress to obligate interactions, many are maintained at the casual or facultative level (Fisher et al. 2017). Thus, important questions arise: how do symbioses evolve from casual to facultative to dependent relationships? When does symbiosis begin (Figure 1.1)?

Figure 1.1 Defining the symbiosis space. X-axis represents the level of interdependency between host and symbiont from casual to facultative to obligate. Y-axis represents the length of the interaction from brief to whole lifecycle. Dotted arrow represents a possible trajectory from free-living to endosymbiotic state.

1.2 Chemical cues mediate symbiotic interactions

The successful establishment of many classic models of horizontally acquired symbiosis (Euprymna-Vibrio; legumes-Rhizobia/mycorrhizal fungi) depend upon successful and specific signal exchanges between partners. Biologists have begun to decipher the chemical languages and cellular and molecular events involved in these exchanges revealing them to be multistage events of some complexity. The complexity of these exchanges strongly suggests that (in their current form) they almost certainly postdate the evolutionary start of the relationship, and likely have limited value in discovering how symbioses develop initially. Furthermore, in the marine environment, most host organisms first interact with multispecies bacterial biofilms as larvae (Lema et al. 2019). How are the “right” signals heard amongst the noise? We argue that examination of pre-symbiotic bacteria–eukaryotic interactions in non-model organisms will greatly enhance our understanding of the interactions and ecological drivers that establish and maintain symbioses.

1.3 How do specific symbiotic interactions begin? Examples from the pre-symbiosis space

Inter-kingdom associations that exist early in the symbiosis continuum (Figure 1.1) can inform our understanding of how symbioses develop. Bacteria can interact with eukaryotes in a number of ways that are not classically defined as symbiosis but result in modifications to the eukaryote’s physiology or behavior. While not strictly symbioses, these interactions can be viewed as existing on the edge of the symbiotic continuum space defined above. For example, rosette (colony) formation and sexual reproduction in choanoflagellates are induced and inhibited by different bacterial metabolites (Levin and King 2013). Rosette formation in Salpingoeca rosetta is induced by a combination of lipid molecules from the prey bacterium Algoriphagus machipongonensis (Alegado et al. 2012; Beemelmanns et al. 2014; Woznica and King 2018). In this example, one form of eukaryotic development is dependent on the presence of appropriate prey microbes; however, the microbes themselves experience only the negative selection pressure of being eaten. Although not a symbiosis, the choanoflagellate example demonstrates how interactions with bacteria can not only drive eukaryotic development but also reveal potential drivers for multicellularity.

Marine sponges and corals provide another valuable space in which to examine not only the interplay between host eukaryotes and their associated bacteria, but also how symbionts can be found amongst the “noise” of diverse bacterial populations. Marine sponges contain diverse consortia of bacteria: currently at least 39 microbial phyla have been demonstrated to associate with sponges (Pita et al. 2018). Additionally, the density of those bacteria can reach 109 microbial cells/cm3 of sponge (Hentschel et al. 2006). The coral microbiome is also a complex consortium: up to 69 phyla have been identified in association with stony corals (Pollock et al. 2018; Huggett and Apprill 2019). In contrast to sponges and corals, most other animals interact with only 3–5 bacterial phyla (Kostic et al. 2013). The natural variability of both microbes and symbioses is reflected in the variability of interactions, from transients to true symbionts, and positive to negative (Figure 1.1). While unravelling the complex mechanisms that allow hosts to identify friend from foe amongst such complex communities remains experimentally challenging (Pita et al. 2016), a number of commonalities are emerging, for example, core groups have been identified that associate with taxonomic consistency (Rohwer et al. 2002; Erwin et al. 2012; Hester et al. 2015; Ainsworth and Gates 2016; Bourne et al. 2016; Thomas et al. 2016; Ainsworth et al. 2017). Many of the identified core microbiomes of these groups have ...

Table of contents

• Cover
• Half Title
• Series Page
• Title Page
• Copyright Page
• Contents
• Series Preface
• Preface
• Contributors
• Chapter 1: When does symbiosis begin? Bacterial cues necessary for metamorphosis in the marine polychaete Hydroides elegans
• Chapter 2: The language of symbiosis: Insights from protist biology
• Chapter 3: Trichoplax and its bacteria: How many are there? Are they speaking?
• Chapter 4: Decoding cellular dialogues between sponges, bacteria, and phages
• Chapter 5: Symbiotic interactions in the holobiont Hydra
• Chapter 6: Hydra and Curvibacter: An intimate crosstalk at the epithelial interface
• Chapter 7: The coral holobiont highlights the dependence of cnidarian animal hosts on their associated microbes
• Chapter 8: Extra-intestinal regulation of the gut microbiome: The case of C. elegans TGFβ/SMA signaling
• Chapter 9: Multiple roles of bacterially produced natural products in the bryozoan Bugula neritina
• Chapter 10: The molecular dialogue through ontogeny between a squid host and its luminous symbiont
• Chapter 11: Evolving integrated multipartite symbioses between plant-sap feeding insects (Hemiptera) and their endosymbionts
• Chapter 12: Symbiosis for insect cuticle formation
• Chapter 13: Microbial determinants of folivory in insects
• Chapter 14: Right on cue: Microbiota promote plasticity of zebrafish digestive tract
• Chapter 15: Uncovering the history of intestinal host–microbiome interactions through vertebrate comparative genomics
• Chapter 16: Molecular interactions of microbes and the plant phyllosphere: The phyllosphere-microbiome is shaped by the interplay of secreted microbial molecules and the plant immune system
• Chapter 17: Cellular dialogues between hosts and microbial symbionts: Generalities emerging
• Index