Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes

Theis, Kevin R.; Dheilly, Nolwenn M.; Klassen, Jonathan L.; Brucker, Robert M.; Baines, John F.; Bosch, Thomas C. G.; Cryan, John F.; Gilbert, Scott F.; Goodnight, Charles J.; Lloyd, Elisabeth A.; Sapp, Jan; Vandenkoornhuyse, Philippe; Zilber‐Rosenberg, Ilana; Rosenberg, Eugene; Bordenstein, Seth R.

doi:10.1128/msystems.00028-16

Cited by 428 publications

(254 citation statements)

References 34 publications

Supporting

Mentioning

248

Contrasting

Unclassified

Order By: Relevance

“…Current theory and research on holobionts are now beginning to explicitly consider the variation in a natural environmental context, in part, because it is a necessary factor to understand the evolution of holobionts and hologenomes (Zilber-Rosenberg and Rosenberg, 2008; Theis et al, 2016). Studies of the host-associated microbial repertoire are useful in the effort to highlight the importance of microbes in host biology (e.g., physiology, development, immunology, behavior, population genetics; Jaenike, 2012; Eisthen and Theis, 2016; Kohl and Carey, 2016; Shropshire and Bordenstein, 2016) and ecology.…”

Section: Expanding Theory On Holobiontsmentioning

confidence: 99%

The Hologenome Across Environments and the Implications of a Host-Associated Microbial Repertoire

Carrier

Reitzel

2017

Front. Microbiol.

View full text Add to dashboard Cite

Our understanding of the diverse interactions between hosts and microbes has grown profoundly over the past two decades and, as a product, has revolutionized our knowledge of the life sciences. Through primarily laboratory experiments, the current framework for holobionts and their respective hologenomes aims to decipher the underpinnings and implications of symbioses between host and microbiome. However, the laboratory setting restricts the full spectrum of host-associated symbionts as compared to those found in nature; thus, limiting the potential for a holistic interpretation of the functional roles the microbiome plays in host biology. When holobionts are studied in nature, associated microbial communities vary considerably between conditions, resulting in more microbial associates as part of the “hologenome” across environments than in either environment alone. We review and synthesize empirical evidence suggesting that hosts may associate with a larger microbial network that, in part, corresponds to experiencing diverse environmental conditions. To conceptualize the interactions between host and microbiome in an ecological context, we suggest the “host-associated microbial repertoire,” which is the sum of microbial species a host may associate with over the course of its life-history under all encountered environmental circumstances. Furthermore, using examples from both terrestrial and marine ecosystems, we discuss how this concept may be used as a framework to compare the ability of the holobiont to acclimate and adapt to environmental variation, and propose three “signatures” of the concept.

show abstract

Section: Expanding Theory On Holobiontsmentioning

confidence: 99%

The Hologenome Across Environments and the Implications of a Host-Associated Microbial Repertoire

Carrier

Reitzel

2017

Front. Microbiol.

View full text Add to dashboard Cite

show abstract

“…The coral microbiome is composed of a diverse assemblage of microorganisms, including algae, other protists, bacteria, archaea, fungi, and viruses, and this consortium is collectively referred to as the holobiont (1–3). Most attention has been dedicated towards studying the dynamics between endosymbiotic algae (generally Symbiodinium ) and corals because the photosynthate provided by these algae is fundamental for the metabolism, calcification, and overall growth of stony corals (4, 5).…”

Section: Introductionmentioning

confidence: 99%

Distinguishing between Microbial Habitats Unravels Ecological Complexity in Coral Microbiomes

2016

View full text Add to dashboard Cite

This study demonstrates that coral tissue or mucus habitats structure the microbiome of corals and that separation of these habitats facilitates identification of consistent microbial associates. Using this approach, we demonstrated that sequences related to “Candidatus Amoebophilus,” recognized intracellular symbionts of amoebae, were highly associated with the tissues of Caribbean corals and possibly endosymbionts of a protistan host within corals, adding a further degree of intricacy to coral holobiont symbioses. Examining specific habitats within complex hosts such as corals is useful for targeting important microbial associations that may otherwise be masked by the sheer microbial diversity associated with all host habitats.

show abstract

“…Taken together with the prevalence of symbiosis in animals and plants, it suggested consider ation of the holobiont as a basic unit of selection in evolution . This claim, however, has been challenged by an opposing view, arguing that the association of hosts with their gut microbiota is typically not strict and selective enough to justify the consideration of holobionts as units of selection . It was further proposed that the effects of interactions and transmission of bacteria can be accommodated by traditional frameworks, without a need to revise the basic foundations of evolution .…”

Section: Introductionmentioning

confidence: 99%

Microbiome‐Germline Interactions and Their Transgenerational Implications

Elgart¹,

Soen²

2017

BioEssays

View full text Add to dashboard Cite

It is becoming increasingly clear that most, if not all, animals and plants are associated with a diverse array of resident gut microbiota. This symbiosis is regulated by host-microbiome interactions which influence the development, homeostasis, adaptation and evolution of the host. Recent evidence indicated that these interactions can also affect the host germline and have a potential of supporting transgenerational effects, including inheritance of acquired characteristics. Taken together, the influence of gut bacteria on the host soma and germline could potentially give rise to emergent phenotypes, which may be partially inherited by three distinguishable modes of transgenerational influence of gut bacteria: 1) "soma-to-soma" 2) "soma-to-germline" and 3) "soma-germline-soma". Here, we discuss these possibilities in light of evidence supporting bacterial-mediated modes of transgenerational inheritance.

show abstract

Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes

Cited by 428 publications

References 34 publications

The Hologenome Across Environments and the Implications of a Host-Associated Microbial Repertoire

The Hologenome Across Environments and the Implications of a Host-Associated Microbial Repertoire

Distinguishing between Microbial Habitats Unravels Ecological Complexity in Coral Microbiomes

Microbiome‐Germline Interactions and Their Transgenerational Implications

Contact Info

Product

Resources

About