Role of Microorganisms in the Evolution of Animals and Plants

A special issue of Microorganisms (ISSN 2076-2607).

Deadline for manuscript submissions: closed (31 August 2020) | Viewed by 49414

Special Issue Editors


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Guest Editor
Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv-Yafo, Israel
Interests: microbiome; holobiont; hologenome; microbiota; corals; evolution
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv-Yafo, Israel
Interests: nutrigenomics; nutrigenetics; metabolism; aging

Special Issue Information

Dear Colleagues,

The concept of microorganisms playing a role in the evolution of animals and plants was suggested because of the realization that all animals and plants harbor diverse microorganisms that affect the fitness of their hosts. Subsequently, interest in this field has grown exponentially, though the dynamics and complexity of microbiomes and their interactions with hosts are only beginning to be understood. This conglomerate of host and its microbes, including bacteria, archaea, protists and viruses, has been termed holobiont, metaorganism, and superorganism. During the last decade, the extent to which host/microbiome interactions affect the fitness of animals and plants has become a major theoretical and applied research topic. Another subject that has attracted attention and been demonstrated in some systems is the transmission of microbiomes and their genes between generations, though the generality of this has been challenged and needs further research. Consideration of the holobiont with its hologenome as a level of selection has led to previously underappreciated modes of genetic variation and evolution that also have to be examined theoretically and experimentally. In this Special Issue, we invite scientists to contribute articles on the different topics associated with the role of microorganisms in the evolution of plant and animal (including human) holobionts with the aim of a better understanding of how these complex systems adapt and evolve.

Prof. Eugene Rosenberg
Dr. Ilana Zilber-Rosenberg
Guest Editors

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Keywords

holobiont

hologenome

microbiome

evolution

plant-host interaction

animal (including human)-host interaction

Published Papers (10 papers)

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Editorial

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4 pages, 178 KiB  
Editorial
Special Issue: The Role of Microorganisms in the Evolution of Animals and Plants
by Eugene Rosenberg and Ilana Zilber-Rosenberg
Microorganisms 2022, 10(2), 250; https://doi.org/10.3390/microorganisms10020250 - 23 Jan 2022
Cited by 2 | Viewed by 2341
Abstract
It is now well established that all animals and plants harbor abundant and diverse microorganisms, including bacteria, archaea, viruses, and eukaryotic microorganisms [...] Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)

Research

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9 pages, 1412 KiB  
Article
Interactions with a Complex Microbiota Mediate a Trade-Off between the Host Development Rate and Heat Stress Resistance
by Samuel Slowinski, Isabella Ramirez, Vivek Narayan, Medha Somayaji, Maya Para, Sarah Pi, Niharika Jadeja, Siavash Karimzadegan, Barbara Pees and Michael Shapira
Microorganisms 2020, 8(11), 1781; https://doi.org/10.3390/microorganisms8111781 - 13 Nov 2020
Cited by 8 | Viewed by 2335
Abstract
Animals and plants host diverse communities of microorganisms, and these microbiotas have been shown to influence host life history traits. Much has been said about the benefits that host-associated microbiotas bestow on the host. However, life history traits often demonstrate tradeoffs among one [...] Read more.
Animals and plants host diverse communities of microorganisms, and these microbiotas have been shown to influence host life history traits. Much has been said about the benefits that host-associated microbiotas bestow on the host. However, life history traits often demonstrate tradeoffs among one another. Raising Caenorhabditis elegans nematodes in compost microcosms emulating their natural environment, we examined how complex microbiotas affect host life history traits. We show that soil microbes usually increase the host development rate but decrease host resistance to heat stress, suggesting that interactions with complex microbiotas may mediate a tradeoff between host development and stress resistance. What element in these interactions is responsible for these effects is yet unknown, but experiments with live versus dead bacteria suggest that such effects may depend on bacterially provided signals. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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19 pages, 2727 KiB  
Article
Salt Marsh Elevation Drives Root Microbial Composition of the Native Invasive Grass Elytrigia atherica
by Edisa García Hernández, Elena Baraza, Christian Smit, Matty P. Berg and Joana Falcão Salles
Microorganisms 2020, 8(10), 1619; https://doi.org/10.3390/microorganisms8101619 - 21 Oct 2020
Cited by 7 | Viewed by 2777
Abstract
Elytrigia atherica is a native invasive plant species whose expansion on salt marshes is attributed to genotypic and phenotypic adaptations to non-ideal environmental conditions, forming two ecotypes. It is unknown how E. atherica–microbiome interactions are contributing to its adaptation. Here we investigated [...] Read more.
Elytrigia atherica is a native invasive plant species whose expansion on salt marshes is attributed to genotypic and phenotypic adaptations to non-ideal environmental conditions, forming two ecotypes. It is unknown how E. atherica–microbiome interactions are contributing to its adaptation. Here we investigated the effect of sea-water flooding frequency and associated soil (a)biotic conditions on plant traits and root-associated microbial community composition and potential functions of two E. atherica ecotypes. We observed higher endomycorrhizal colonization in high-elevation ecotypes (HE, low inundation frequency), whereas low-elevation ecotypes (LE, high inundation frequency) had higher specific leaf area. Similarly, rhizosphere and endosphere bacterial communities grouped according to ecotypes. Soil ammonium content and elevation explained rhizosphere bacterial composition. Around 60% the endosphere amplicon sequence variants (ASVs) were also found in soil and around 30% of the ASVs were ecotype-specific. The endosphere of HE-ecotype harbored more unique sequences than the LE-ecotype, the latter being abundant in halophylic bacterial species. The composition of the endosphere may explain salinity and drought tolerance in relation to the local environmental needs of each ecotype. Overall, these results suggest that E. atherica is flexible in its association with soil bacteria and ecotype-specific dissimilar, which may enhance its competitive strength in salt marshes. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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20 pages, 3898 KiB  
Article
The Complexity of the Holobiont in the Red Sea Coral Euphyllia paradivisa under Heat Stress
by Dalit Meron, Keren Maor-Landaw, Gal Eyal, Hila Elifantz, Ehud Banin, Yossi Loya and Oren Levy
Microorganisms 2020, 8(3), 372; https://doi.org/10.3390/microorganisms8030372 - 6 Mar 2020
Cited by 5 | Viewed by 4345
Abstract
The recognition of the microbiota complexity and their role in the evolution of their host is leading to the popularization of the holobiont concept. However, the coral holobiont (host and its microbiota) is still enigmatic and unclear. Here, we explore the complex relations [...] Read more.
The recognition of the microbiota complexity and their role in the evolution of their host is leading to the popularization of the holobiont concept. However, the coral holobiont (host and its microbiota) is still enigmatic and unclear. Here, we explore the complex relations between different holobiont members of a mesophotic coral Euphyllia paradivisa. We subjected two lines of the coral—with photosymbionts, and without photosymbionts (apo-symbiotic)—to increasing temperatures and to antibiotics. The different symbiotic states were characterized using transcriptomics, microbiology and physiology techniques. The bacterial community’s composition is dominated by bacteroidetes, alphaproteobacteria, and gammaproteobacteria, but is dependent upon the symbiont state, colony, temperature treatment, and antibiotic exposure. Overall, the most important parameter determining the response was whether the coral was a symbiont/apo-symbiotic, while the colony and bacterial composition were secondary factors. Enrichment Gene Ontology analysis of coral host’s differentially expressed genes demonstrated the cellular differences between symbiotic and apo-symbiotic samples. Our results demonstrate the significance of each component of the holobiont consortium and imply a coherent link between them, which dramatically impacts the molecular and cellular processes of the coral host, which possibly affect its fitness, particularly under environmental stress. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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11 pages, 703 KiB  
Article
Drosophila Sexual Attractiveness in Older Males Is Mediated by Their Microbiota
by Chloe Heys, Anne Lizé, Zenobia Lewis and Tom A. R. Price
Microorganisms 2020, 8(2), 168; https://doi.org/10.3390/microorganisms8020168 - 24 Jan 2020
Cited by 7 | Viewed by 3559
Abstract
Age is well known to be a basis for female preference of males. However, the mechanisms underlying age-based choices are not well understood, with several competing theories and little consensus. The idea that the microbiota can affect host mate choice is gaining traction, [...] Read more.
Age is well known to be a basis for female preference of males. However, the mechanisms underlying age-based choices are not well understood, with several competing theories and little consensus. The idea that the microbiota can affect host mate choice is gaining traction, and in this study we examine whether the male microbiota influences female preference for older individuals in the fruit fly Drosophila pseudoobscura. We find that an intact microbiota is a key component of attractiveness in older males. However, we found no evidence that this decrease in older male attractiveness was simply due to impaired microbiota generally reducing male quality. Instead, we suggest that the microbiota underlies an honest signal used by females to assess male age, and that impaired microbiota disrupt this signal. This suggests that age-based preferences may break down in environments where the microbiota is impaired, for example when individuals are exposed to naturally occurring antibiotics, extreme temperatures, or in animals reared in laboratories on antibiotic supplemented diet. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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15 pages, 2573 KiB  
Article
Tissue- and Population-Level Microbiome Analysis of the Wasp Spider Argiope bruennichi Identified a Novel Dominant Bacterial Symbiont
by Monica M. Sheffer, Gabriele Uhl, Stefan Prost, Tillmann Lueders, Tim Urich and Mia M. Bengtsson
Microorganisms 2020, 8(1), 8; https://doi.org/10.3390/microorganisms8010008 - 19 Dec 2019
Cited by 20 | Viewed by 8193
Abstract
Many ecological and evolutionary processes in animals depend upon microbial symbioses. In spiders, the role of the microbiome in these processes remains mostly unknown. We compared the microbiome between populations, individuals, and tissue types of a range-expanding spider, using 16S rRNA gene sequencing. [...] Read more.
Many ecological and evolutionary processes in animals depend upon microbial symbioses. In spiders, the role of the microbiome in these processes remains mostly unknown. We compared the microbiome between populations, individuals, and tissue types of a range-expanding spider, using 16S rRNA gene sequencing. Our study is one of the first to go beyond targeting known endosymbionts in spiders and characterizes the total microbiome across different body compartments (leg, prosoma, hemolymph, book lungs, ovaries, silk glands, midgut, and fecal pellets). Overall, the microbiome differed significantly between populations and individuals, but not between tissue types. The microbiome of the wasp spider Argiope bruennichi features a novel dominant bacterial symbiont, which is abundant in every tissue type in spiders from geographically distinct populations and that is also present in offspring. The novel symbiont is affiliated with the Tenericutes, but has low sequence identity (<85%) to all previously named taxa, suggesting that the novel symbiont represents a new bacterial clade. Its presence in offspring implies that it is vertically transmitted. Our results shed light on the processes that shape microbiome differentiation in this species and raise several questions about the implications of the novel dominant bacterial symbiont on the biology and evolution of its host. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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Review

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24 pages, 450 KiB  
Review
Reconstitution and Transmission of Gut Microbiomes and Their Genes between Generations
by Eugene Rosenberg and Ilana Zilber-Rosenberg
Microorganisms 2022, 10(1), 70; https://doi.org/10.3390/microorganisms10010070 - 30 Dec 2021
Cited by 15 | Viewed by 3294
Abstract
Microbiomes are transmitted between generations by a variety of different vertical and/or horizontal modes, including vegetative reproduction (vertical), via female germ cells (vertical), coprophagy and regurgitation (vertical and horizontal), physical contact starting at birth (vertical and horizontal), breast-feeding (vertical), and via the environment [...] Read more.
Microbiomes are transmitted between generations by a variety of different vertical and/or horizontal modes, including vegetative reproduction (vertical), via female germ cells (vertical), coprophagy and regurgitation (vertical and horizontal), physical contact starting at birth (vertical and horizontal), breast-feeding (vertical), and via the environment (horizontal). Analyses of vertical transmission can result in false negatives (failure to detect rare microbes) and false positives (strain variants). In humans, offspring receive most of their initial gut microbiota vertically from mothers during birth, via breast-feeding and close contact. Horizontal transmission is common in marine organisms and involves selectivity in determining which environmental microbes can colonize the organism’s microbiome. The following arguments are put forth concerning accurate microbial transmission: First, the transmission may be of functions, not necessarily of species; second, horizontal transmission may be as accurate as vertical transmission; third, detection techniques may fail to detect rare microbes; lastly, microbiomes develop and reach maturity with their hosts. In spite of the great variation in means of transmission discussed in this paper, microbiomes and their functions are transferred from one generation of holobionts to the next with fidelity. This provides a strong basis for each holobiont to be considered a unique biological entity and a level of selection in evolution, largely maintaining the uniqueness of the entity and conserving the species from one generation to the next. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
13 pages, 539 KiB  
Review
The Coevolution of Plants and Microbes Underpins Sustainable Agriculture
by Dongmei Lyu, Levini A. Msimbira, Mahtab Nazari, Mohammed Antar, Antoine Pagé, Ateeq Shah, Nadia Monjezi, Jonathan Zajonc, Cailun A. S. Tanney, Rachel Backer and Donald L. Smith
Microorganisms 2021, 9(5), 1036; https://doi.org/10.3390/microorganisms9051036 - 12 May 2021
Cited by 34 | Viewed by 6332
Abstract
Terrestrial plants evolution occurred in the presence of microbes, the phytomicrobiome. The rhizosphere microbial community is the most abundant and diverse subset of the phytomicrobiome and can include both beneficial and parasitic/pathogenic microbes. Prokaryotes of the phytomicrobiome have evolved relationships with plants that [...] Read more.
Terrestrial plants evolution occurred in the presence of microbes, the phytomicrobiome. The rhizosphere microbial community is the most abundant and diverse subset of the phytomicrobiome and can include both beneficial and parasitic/pathogenic microbes. Prokaryotes of the phytomicrobiome have evolved relationships with plants that range from non-dependent interactions to dependent endosymbionts. The most extreme endosymbiotic examples are the chloroplasts and mitochondria, which have become organelles and integral parts of the plant, leading to some similarity in DNA sequence between plant tissues and cyanobacteria, the prokaryotic symbiont of ancestral plants. Microbes were associated with the precursors of land plants, green algae, and helped algae transition from aquatic to terrestrial environments. In the terrestrial setting the phytomicrobiome contributes to plant growth and development by (1) establishing symbiotic relationships between plant growth-promoting microbes, including rhizobacteria and mycorrhizal fungi, (2) conferring biotic stress resistance by producing antibiotic compounds, and (3) secreting microbe-to-plant signal compounds, such as phytohormones or their analogues, that regulate aspects of plant physiology, including stress resistance. As plants have evolved, they recruited microbes to assist in the adaptation to available growing environments. Microbes serve themselves by promoting plant growth, which in turn provides microbes with nutrition (root exudates, a source of reduced carbon) and a desirable habitat (the rhizosphere or within plant tissues). The outcome of this coevolution is the diverse and metabolically rich microbial community that now exists in the rhizosphere of terrestrial plants. The holobiont, the unit made up of the phytomicrobiome and the plant host, results from this wide range of coevolved relationships. We are just beginning to appreciate the many ways in which this complex and subtle coevolution acts in agricultural systems. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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12 pages, 716 KiB  
Review
Plant Holobiont Theory: The Phytomicrobiome Plays a Central Role in Evolution and Success
by Dongmei Lyu, Jonathan Zajonc, Antoine Pagé, Cailun A. S. Tanney, Ateeq Shah, Nadia Monjezi, Levini A. Msimbira, Mohammed Antar, Mahtab Nazari, Rachel Backer and Donald L. Smith
Microorganisms 2021, 9(4), 675; https://doi.org/10.3390/microorganisms9040675 - 24 Mar 2021
Cited by 54 | Viewed by 8583
Abstract
Under natural conditions, plants are always associated with a well-orchestrated community of microbes—the phytomicrobiome. The nature and degree of microbial effect on the plant host can be positive, neutral, or negative, and depends largely on the environment. The phytomicrobiome is integral for plant [...] Read more.
Under natural conditions, plants are always associated with a well-orchestrated community of microbes—the phytomicrobiome. The nature and degree of microbial effect on the plant host can be positive, neutral, or negative, and depends largely on the environment. The phytomicrobiome is integral for plant growth and function; microbes play a key role in plant nutrient acquisition, biotic and abiotic stress management, physiology regulation through microbe-to-plant signals, and growth regulation via the production of phytohormones. Relationships between the plant and phytomicrobiome members vary in intimacy, ranging from casual associations between roots and the rhizosphere microbial community, to endophytes that live between plant cells, to the endosymbiosis of microbes by the plant cell resulting in mitochondria and chloroplasts. If we consider these key organelles to also be members of the phytomicrobiome, how do we distinguish between the two? If we accept the mitochondria and chloroplasts as both members of the phytomicrobiome and the plant (entrained microbes), the influence of microbes on the evolution of plants becomes so profound that without microbes, the concept of the “plant” is not viable. This paper argues that the holobiont concept should take greater precedence in the plant sciences when referring to a host and its associated microbial community. The inclusivity of this concept accounts for the ambiguous nature of the entrained microbes and the wide range of functions played by the phytomicrobiome in plant holobiont homeostasis. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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Other

22 pages, 383 KiB  
Concept Paper
Toward a Symbiotic Perspective on Public Health: Recognizing the Ambivalence of Microbes in the Anthropocene
by Salla Sariola and Scott F. Gilbert
Microorganisms 2020, 8(5), 746; https://doi.org/10.3390/microorganisms8050746 - 16 May 2020
Cited by 21 | Viewed by 5139
Abstract
Microbes evolve in complex environments that are often fashioned, in part, by human desires. In a global perspective, public health has played major roles in structuring how microbes are perceived, cultivated, and destroyed. The germ theory of disease cast microbes as enemies of [...] Read more.
Microbes evolve in complex environments that are often fashioned, in part, by human desires. In a global perspective, public health has played major roles in structuring how microbes are perceived, cultivated, and destroyed. The germ theory of disease cast microbes as enemies of the body and the body politic. Antibiotics have altered microbial development by providing stringent natural selection on bacterial species, and this has led to the formation of antibiotic-resistant bacterial strains. Public health perspectives such as “Precision Public Health” and “One Health” have recently been proposed to further manage microbial populations. However, neither of these take into account the symbiotic relationships that exist between bacterial species and between bacteria, viruses, and their eukaryotic hosts. We propose a perspective on public health that recognizes microbial evolution through symbiotic associations (the hologenome theory) and through lateral gene transfer. This perspective has the advantage of including both the pathogenic and beneficial interactions of humans with bacteria, as well as combining the outlook of the “One Health” model with the genomic methodologies utilized in the “Precision Public Health” model. In the Anthropocene, the conditions for microbial evolution have been altered by human interventions, and public health initiatives must recognize both the beneficial (indeed, necessary) interactions of microbes with their hosts as well as their pathogenic interactions. Full article
(This article belongs to the Special Issue Role of Microorganisms in the Evolution of Animals and Plants)
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