John Tyler Bonner's call to re‐evaluate evolutionary theory in light of major transitions in life on Earth (e.g., from the first origins of microbial life to the evolution of sex, and the origins of multicellularity) resonate with recent discoveries on epigenetics and the concept of the hologenome. Current studies of genome evolution often mistakenly focus only on the inheritance of DNA between parent and offspring. These are in line with the widely accepted Neo‐Darwinian framework that pairs Mendelian genetics with an emphasis on natural selection as explanations for the evolution of biodiversity on Earth. Increasing evidence for widespread symbioses complicates this narrative, as is seen in Scott Gilbert's discussion of the concept of the holobiont in this series: Organisms across the tree of life coexist with substantial influence on one another through endosymbiosis, symbioses, and host‐associated microbiomes. The holobiont theory, coupled with observations from molecular studies, also requires us to understand genomes in a new way—by considering the interactions underlain by the genome of a host plus its associated microbes, a conglomerate entity referred to as the hologenome. We argue that the complex patterns of inheritance of these genomes coupled with the influence of symbionts on host gene expression make the concept of the hologenome an epigenetic phenomenon. We further argue that the aspects of the hologenome challenge of the modern evolutionary synthesis, which requires updating to remain consistent with Darwin's intent of providing natural laws that underlie the evolution of life on Earth.
- Award ID(s):
- 1851085
- NSF-PAR ID:
- 10148988
- Date Published:
- Journal Name:
- F1000Research
- Volume:
- 7
- ISSN:
- 2046-1402
- Page Range / eLocation ID:
- 1664
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
Microbiomes of the Sydney Rock Oyster are acquired through both vertical and horizontal transmissionmore » « less
Abstract Background The term holobiont is widely accepted to describe animal hosts and their associated microorganisms. The genomes of all that the holobiont encompasses, are termed the hologenome and it has been proposed as a unit of selection in evolution. To demonstrate that natural selection acts on the hologenome, a significant portion of the associated microbial genomes should be transferred between generations. Using the Sydney Rock Oyster (
Saccostrea glomerata ) as a model, we tested if the microbes of this broadcast spawning species could be passed down to the next generation by conducting single parent crosses and tracking the microbiome from parent to offspring and throughout early larval stages using 16S rRNA gene amplicon sequencing. From each cross, we sampled adult tissues (mantle, gill, stomach, gonad, eggs or sperm), larvae (D-veliger, umbo, eyed pediveliger, and spat), and the surrounding environment (water and algae feed) for microbial community analysis.Results We found that each larval stage has a distinct microbiome that is partially influenced by their parental microbiome, particularly the maternal egg microbiome. We also demonstrate the presence of core microbes that are consistent across all families, persist throughout early life stages (from eggs to spat), and are not detected in the microbiomes of the surrounding environment. In addition to the core microbiomes that span all life cycle stages, there is also evidence of environmentally acquired microbial communities, with earlier larval stages (D-veliger and umbo), more influenced by seawater microbiomes, and later larval stages (eyed pediveliger and spat) dominated by microbial members that are specific to oysters and not detected in the surrounding environment.
Conclusion Our study characterized the succession of oyster larvae microbiomes from gametes to spat and tracked selected members that persisted across multiple life stages. Overall our findings suggest that both horizontal and vertical transmission routes are possible for the complex microbial communities associated with a broadcast spawning marine invertebrate. We demonstrate that not all members of oyster-associated microbiomes are governed by the same ecological dynamics, which is critical for determining what constitutes a hologenome.
-
more » « less
Summary Holobiont phenotype results from a combination of host and symbiont genotypes as well as from prevailing environmental conditions that alter the relationships among symbiotic members. Corals exemplify this concept, where shifts in the algal symbiont community can lead to some corals becoming more or less thermally tolerant. Despite linkage between coral bleaching and disease, the roles of symbiotic bacteria in holobiont resistance and susceptibility to disease remains less well understood. This study thus characterizes the microbiome of disease‐resistant and ‐susceptible
Acropora cervicornis coral genotypes (hereafter referred to simply as ‘genotypes’) before and after high temperature‐mediated bleaching. We found that the intracellular bacterial parasite ‘Ca. Aquarickettsia rohweri’ was strikingly abundant in disease‐susceptible genotypes. Disease‐resistant genotypes, however, had notably more diverse and even communities, with correspondingly low abundances of ‘Ca. Aquarickettsia’. Bleaching caused a dramatic reduction of ‘Ca. Aquarickettsia’ within disease‐susceptible corals and led to an increase in bacterial community dispersion, as well as the proliferation of opportunists. Our data support the hypothesis that ‘Ca. Aquarickettsia’ species increase coral disease risk through two mechanisms: (i) the creation of host nutritional deficiencies leading to a compromised host‐symbiont state and (ii) the opening of niche space for potential pathogens during thermal stress. -
Wilson, Daniel ; Parkhill, Julian (Ed.)ABSTRACT A goal of modern biology is to develop the genotype-phenotype (G→P) map, a predictive understanding of how genomic information generates trait variation that forms the basis of both natural and managed communities. As microbiome research advances, however, it has become clear that many of these traits are symbiotic extended phenotypes , being governed by genetic variation encoded not only by the host’s own genome, but also by the genomes of myriad cryptic symbionts. Building a reliable G→P map therefore requires accounting for the multitude of interacting genes and even genomes involved in symbiosis. Here, we use naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti paired with two genotypes of the host Medicago truncatula in four genome-wide association studies (GWAS) to determine the genomic architecture of a key symbiotic extended phenotype— partner quality , or the fitness benefit conferred to a host by a particular symbiont genotype, within and across environmental contexts and host genotypes. We define three novel categories of loci in rhizobium genomes that must be accounted for if we want to build a reliable G→P map of partner quality; namely, (i) loci whose identities depend on the environment, (ii) those that depend on the host genotype with which rhizobia interact, and (iii) universal loci that are likely important in all or most environments. IMPORTANCE Given the rapid rise of research on how microbiomes can be harnessed to improve host health, understanding the contribution of microbial genetic variation to host phenotypic variation is pressing, and will better enable us to predict the evolution of (and select more precisely for) symbiotic extended phenotypes that impact host health. We uncover extensive context-dependency in both the identity and functions of symbiont loci that control host growth, which makes predicting the genes and pathways important for determining symbiotic outcomes under different conditions more challenging. Despite this context-dependency, we also resolve a core set of universal loci that are likely important in all or most environments, and thus, serve as excellent targets both for genetic engineering and future coevolutionary studies of symbiosis.more » « less
-
Effective coral restoration must include comprehensive investigations of the targeted coral community that consider all aspects of the coral holobiont—the coral host, symbiotic algae, and microbiome. For example, the richness and composition of microorganisms associated with corals may be indicative of the corals’ health status and thus help guide restoration activities. Potential differences in microbiomes of restoration corals due to differences in host genetics, environmental condition, or geographic location, may then influence outplant success. The objective of the present study was to characterize and compare the microbiomes of apparently healthy Acropora cervicornis genotypes that were originally collected from environmentally distinct regions of Florida’s Coral Reef and sampled after residing within Mote Marine Laboratory’s in situ nursery near Looe Key, FL (USA) for multiple years. By using 16S rRNA high-throughput sequencing, we described the microbial communities of 74 A. cervicornis genotypes originating from the Lower Florida Keys ( n = 40 genotypes), the Middle Florida Keys ( n = 15 genotypes), and the Upper Florida Keys ( n = 19 genotypes). Our findings demonstrated that the bacterial communities of A. cervicornis originating from the Lower Keys were significantly different from the bacterial communities of those originating from the Upper and Middle Keys even after these corals were held within the same common garden nursery for an average of 3.4 years. However, the bacterial communities of corals originating in the Upper Keys were not significantly different from those in the Middle Keys. The majority of the genotypes, regardless of collection region, were dominated by Alphaproteobacteria, namely an obligate intracellular parasite of the genus Ca. Aquarickettsia . Genotypes from the Upper and Middle Keys also had high relative abundances of Spirochaeta bacteria. Several genotypes originating from both the Lower and Upper Keys had lower abundances of Aquarickettsia , resulting in significantly higher species richness and diversity. Low abundance of Aquarickettsia has been previously identified as a signature of disease resistance. While the low- Aquarickettsia corals from both the Upper and Lower Keys had high abundances of an unclassified Proteobacteria, the genotypes in the Upper Keys were also dominated by Spirochaeta . The results of this study suggest that the abundance of Aquarickettsia and Spirochaeta may play an important role in distinguishing bacterial communities among A. cervicornis populations and compositional differences of these bacterial communities may be driven by regional processes that are influenced by both the environmental history and genetic relatedness of the host. Additionally, the high microbial diversity of low- Aquarickettsia genotypes may provide resilience to their hosts, and these genotypes may be a potential resource for restoration practices and management.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.12688/f1000research.14385.1
