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Editorial: Epigenetics as a Deep Intimate Dialogue between Host and Symbionts
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Abstract
Host-symbiont epigenetic crosstalk: A “koiné language” that enables communication
between different species
In ancient Greek, the term koiné refers to a common language, which spread in the
Eastern Mediterranean region and the Near East following the conquests of Alexander
the Great. In the 4th century BC, koiné quickly became a shared language that enabled
people speaking different dialects to communicate with each other. Indeed, effective
communication is always necessary for overcoming “barriers” between individuals and
groups, tightening relationships, and enabling new ways of coping with a changing
world. This is the case not only for interactions involving cultural relations. Different
living entities communicate in many ways, with the most intimate and often the most
long-lasting communication being the formation of mutually beneficial, obligatory
symbiotic associations. As Lynn Margulis forcefully argued, symbiotic relations are
found among virtually all living organisms, and were critical for the origin and diversification
of the eukaryotes (Sagan, 1967; Margulis, 1971; Guerrero et al., 2013). Since the
partners in symbiotic relationships frequently belong to different kingdoms, and the
intimacy may be so deep that the Symbionts reside in the tissues and/or cells of the
host, their shared “language” should be a basic—and ancient—form of communication.
Such effective communication blurs the boundaries between different living entities,
giving rise to a single biomolecular network, a “holobiont” with a “hologenome” (Zilber-Rosenberg
and Rosenberg, 2008; Bordenstein and Theis, 2015), thus problematizing the conventional
notion of individuality. The series of papers presented in this topic-issue explore
the fascinating developmental and evolutionary relationship between Symbionts and
hosts, by focusing on the mediating epigenetic processes that enable the communication
to be effective and robust at both the individual, the ecological, and the evolutionary
time scales.
One of the currently most researched cases illustrating the productive cross-talk
between Symbionts and hosts is the symbiosis between mammals and their gut microbiome.
As Gilbert stresses, the birth of a mammal is not merely the origin of a new distinct
(traditional) individual, but the onset of a new community. Already in utero, the
fetus interacts with a network of symbiotic factors that is provided by the mother
and, at birth, as it leaves the maternal symbiotic association system, it forms its
own community which, although largely based on the legacy it gets from its mother,
becomes rapidly adapted to its specific idiosyncratic conditions of life. Since the
normal development and the thriving of the newborn depend on the symbiotic legacy
it receives, it is the holobiont—the community of interacting species—that is the
target of both developmental and natural selection. However, as Fridmann-Sirkis et
al. illustrate, in extreme circumstances, when interactions fail, for example, because
of acute stress to the microbiome, the host adapts by making adaptive changes in its
epigenome, which can be inherited by subsequent generations. In more normal conditions,
the maternal legacy provides crucial developmental resources, and is the basis on
which flexible, context-sensitive, modifications of these resources, that allow rapid
adaptation to the normally dynamic and fluctuating conditions in which the new individual
lives, are constructed.
Since the microbiome reacts and evolutionarily adapts much faster than the host, most
host's physiological adaptations are likely to be initiated by evolutionary changes
to the constitution of the microbiome. Soen analyzes the manner in which the changes
in the constitution of the microbiome lead to the modification of the communication
process among the species comprising the microbiome, as well as between the microbiome
and the host; and shows how these changes enable the developmental construction of
a new dynamic, adaptive equilibrium, involving mutually beneficial epigenetic modifications
in the host that can be epigenetically inherited between host generations. Hence,
adaptive evolutionary modifications in the rapidly evolving microbiome, that occur
at the time scale of host's individual life, are followed by the epigenetic inheritance
of the host's physiological adaptations, thus enabling adaptive adjustments of the
host at the ecological time scale (Soen; see also Moran and Sloan, 2015).
Although many symbiotic associations play essential roles in host development, physiology,
and health, some associations may be harmful for the host. In these cases, the “selfish”
Symbiont (often referred to as “parasite”) must evade the host's immune responses,
and this may occur through “misleading” the host, for example, by mimicking the host's
signaling and control system for its own benefits. Some intracellular pathogenic bacteria,
such as Anaplasma phagocytophilum a pathogen studied by Sinclair et al. encode eukaryotic-like
proteins (e.g., the nucleomodulin AnkA) for subverting the host cells metabolism by
recruiting chromatin-modifying enzymes or by altering the folding patterns of chromatin
that bring distant regulatory regions together to coordinate control of transcriptional
reprogramming. Other epigenetic factors are SET-domain containing proteins, which
are known to modify chromatin structure in eukaryotic cells. Alvarez-Venegas shows
that SET domain genes, which meditate host-symbiont epigenetic interactions, and that
have been identified in several bacterial genomes on the basis of their similarity
to the SET domains of eukaryotic histone methyltransferases, allow pathogens to inhibit
transcriptional activation of host defense genes. Indeed, there is plenty of evidence
supporting the role of epigenetic mechanisms (e.g., DNA methylation, mechanisms that
re-model chromatin structure through histone modifications, and mechanisms underlying
RNA interference) both in pathogen plasticity and pathogen-induced alterations of
the host (Gómez-Díaz et al., 2012). One such example is the molecular pathogenesis
of Epstein–Barr virus (which induces diverse lymphoid and epithelial malignancies)
discussed by Niller et al. that is accompanied by epigenetic alterations of both the
viral and the host genomes.
Some “parasites” promote genetic exchange with the host genome. According to many
studies, the exchange of human and viral genes must have happened repeatedly during
evolution, and this can account for the high degree of homology between many viral
and human genes. Niller et al. point to the example of the thymidylate synthase gene
in the genome of Herpesvirus saimiri, which has 70% amino acids homology to that of
the human gene, and Shapiro reviews and discusses the already massive and still growing
evidence showing that such invasions into a host genome through virally-transmitted
genetic elements (transposons, retrotransposons, and genomic proviruses) rewire the
hosts' genomic networks, rearrange the host's genome and exert new types of selection
pressures on it. The evolution of epigenetic silencing strategies, that prevent mobile
DNA from destroying the integrity of the host genome and that have epigenetic heritable
effects, is one such genomic adaptation. Indeed, it has been argued that one of the
main functions of epigenetic mechanisms is a form of “genome immunity,” promoting
protection against foreign genetic elements. Sagy et al. suggest that this cellular
immune function may explain the systematic failure of cloning some eukaryotic genomes
in bacteria. For example, about 20% of the nematode Caenorhabditis elegans genome
is not clonable in Escherichia coli, but can be cloned in yeast, a eukaryote. Interestingly,
the bacterially unclonable sequences are enriched with repetitive DNA transposons
and PIWI-interacting small RNAs (piRNAs). In worms and many other organisms (other
animals and protists), piRNA-mediated RNA interference has a role in genome surveillance
against foreign sequences. Sagy et al. therefore propose that piRNAs may act in trans
to eliminate bacteria (E. coli), thus preventing its ability to be cloned within the
bacterium. As they note, this role of piRNAs may have therapeutic applications, and
could be used against pathogenic bacteria. Another potential epigenetic- medical intervention
can be based on a genome-wide profiling of histone modifications combined with gene
expression in the human malaria vector Anopheles gambiae. Targeting changes in histone
modification and transcription of genes that regulate malaria transmission may provide,
as Gómez-Díaz et al. point out, new type of malaria control. Deciphering the mechanisms
underlying the molecular “dialogue” between hosts and symbionts therefore seems of
major importance for many research areas including medicine, genetics, cell biology,
zoology, microbiology, evolutionary biology, and ecology.
Concluding remarks and perspectives
The papers published in this topic-issue, which focus on the role of epigenetic factors
and mechanisms in the interactions among the different species comprising the holobiont,
point to important research directions. Epigenetic mechanisms enable dynamic developmental
communication, an epigenetic koiné, between hosts and symbionts at several different
time scales. We are confident that the molecular-epigenetic technologies already available—and
those that are rapidly being developed—will provide important insights into the evolution
and development of the organisms on our planet, whose history and future are based
on ongoing communication and interactions.
Author contributions
All authors listed have made substantial, direct and intellectual contribution to
the work, and approved it for publication.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.
Related collections
Most cited references 2
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The origin of plant and animal cells.
L Margulis (1971)
Author and article information
Contributors
Journal
Front Genet
Front Genet
Front. Genet.
Frontiers in Genetics
Frontiers Media S.A.
1664-8021
09
February
2016
2016
: 7
Affiliations
Author notes
Article
10.3389/fgene.2016.00007
4746242
26904096
Copyright © 2016 Negri and Jablonka.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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Editorial