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Posted ContentDOI

Transmission efficiency drives host-microbe associations

24 Jul 2020-bioRxiv (Cold Spring Harbor Laboratory)-
TL;DR: The study reveals that transmission mode is of key importance in establishing host-microbe associations.
Abstract: Sequencing technologies have fueled a rapid rise in descriptions of microbial communities associated with hosts, but what is often harder to ascertain is their evolutionary significance. Here we review the existing literature on the role of vertical (VT), horizontal (HT), environmental acquisition, and mixed modes (MMT) of transmission for establishing animal host-microbe associations. We then modelled four properties of gut microbiota proposed as key to promoting animal host-microbe relationships: modes of transmission, host reproductive mode, host mate choice, and host fitness. We found: (i) MMT led to the highest frequencies of host-microbe associations, and some environmental acquisition or HT of microbes was required for persistent associations to form unless VT was perfect; (ii) host reproductive mode (sexual vs asexual) and host mate choice (for microbe carriers vs non-carriers) had little impact on the establishment of host-microbe associations; (iii) host mate choice did not itself lead to reproductive isolation, but could reinforce it; (iv) changes in host fitness due to host-microbe associations had a minimal impact upon the formation of co-associations. When we introduced a second population, into which host-microbe carriers could disperse but in which environmental acquisition did not occur, highly efficient VT was required for host-microbe co-associations to persist. Our study reveals that transmission mode is of key importance in establishing host-microbe associations.
Citations
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Posted ContentDOI
11 Jan 2022-bioRxiv
TL;DR: The hypothesis that the asymmetry between females and males, together with the hazards that come with biparental transmission of the milk microbiome, generate selection against male lactation in humans, and in mammals in general is put forward.
Abstract: Gut microbiomes of humans carry a complex symbiotic assemblage of microorganisms. As in all mammals, the special mode of feeding newborn infants through milk from the mammary gland enhances the opportunity for vertical transmission of the milk microbiome from parents to the gut microbiome of offspring. This has potential benefits, but it also brings with it some hazards for the host. Here we use mathematical and numerical models to demonstrate that vertical transmission from both parents would allow host populations to be invaded by microbiome elements that are deleterious. In contrast, vertical transmission, when restricted to one parent, acts as a sieve preventing the spread of such elements. We show that deleterious symbionts generate selection for uniparental transmission in host populations, and that this selective advantage is maintained in the presence of moderate horizontal transmission. Some vertical transmission from mother to infant is bound to happen in placental mammals. This paper therefore puts forward the hypothesis that the asymmetry between females and males, together with the hazards that come with biparental transmission of the milk microbiome, generate selection against male lactation in humans, and in mammals in general.

2 citations

Journal ArticleDOI
TL;DR: A mathematical model is developed to identify the conditions under which the mutualist can persist in a population where vertical transmission is imperfect and shows that several factors compensate for imperfect vertical transmission, namely, a selective advantage to the host conferred by the Mutualist, horizontal transmission of the mutualists through an environmental reservoir and transmission of a cultural practice that promotes microbial transmission.
Abstract: Abstract Abstract Humans harbour diverse microbial communities, and this interaction has fitness consequences for hosts and symbionts. Understanding the mechanisms that preserve host–symbiont association is an important step in studying co-evolution between humans and their mutualist microbial partners. This association is promoted by vertical transmission, which is known to be imperfect. It is unclear whether host–microbial associations can generally be maintained despite ‘leaky’ vertical transmission. Cultural practices of the host are expected to be important in bacterial transmission as they influence the host's interaction with other individuals and with the environment. There is a need to understand whether and how cultural practices affect host–microbial associations. Here, we develop a mathematical model to identify the conditions under which the mutualist can persist in a population where vertical transmission is imperfect. We show with this model that several factors compensate for imperfect vertical transmission, namely, a selective advantage to the host conferred by the mutualist, horizontal transmission of the mutualist through an environmental reservoir and transmission of a cultural practice that promotes microbial transmission. By making the host–microbe association more likely to persist in the face of leaky vertical transmission, these factors strengthen the association which in turn enables host–mutualist co-evolution.

2 citations

TL;DR:
Abstract: 17 Mutualistic co-evolution can be mediated by vertical transmission of symbionts between host 18 generations. Organisms exhibit adaptations that ensure optimal microbial inheritance, yet it is 19 unknown if this extends to superorganismal social insects that host co-evolved gut 20 microbiomes. Here, we document consistent vertical transmission that preserves more than 80 21 bacterial genera across colony generations in a fungus-farming termite model system. 22 Inheritance is governed by reproductives, analogous to organismal gametes, that found new 23 colonies and are endowed with environmentally-sensitive and termite-specific gut microbes. 24 These symbionts are then reliably passed on within the offspring colony, where priority effects 25 dictate the composition of the forming colony microbiome. Founding reproductives thus play 26 a central role in transmission. However, in sharp contrast to organismal inheritance of an 27 endosymbiont within an egg, the multicellular properties of the superorganismal gametes

2 citations

Posted ContentDOI
01 Feb 2023-bioRxiv
TL;DR: In this paper , the authors used 16s rRNA amplicon sequencing and source-tracker analyses to reveal how the distinct origins of transmission (maternal, paternal, and horizontal) shaped the juvenile internal and external microbiome establishment in the broad-nosed pipefish Syngnathus typhle.
Abstract: Early life microbial colonizers shape and support the immature vertebrate immune system. Microbial colonization relies on the vertical route via parental provisioning and the horizontal route via environmental contribution. Vertical transmission is mostly a maternal trait making it hard to determine the source of microbial colonization in order to gain insight in the establishment of the microbial community during crucial development stages. The evolution of unique male pregnancy in pipefishes and seahorses enables the disentanglement of both horizontal and vertical transmission, but also facilitates the differentiation of maternal vs. paternal provisioning ranging from egg development, to male pregnancy and early juvenile development. Using 16s rRNA amplicon sequencing and source-tracker analyses, we revealed how the distinct origins of transmission (maternal, paternal & horizontal) shaped the juvenile internal and external microbiome establishment in the broad-nosed pipefish Syngnathus typhle. Paternal provisioning mainly shaped the juvenile external microbiome, whereas maternal microbes were the main source of the internal juvenile microbiome, later developing into the gut microbiome. This suggests that stability of niche microbiomes may vary depending on the route and time point of colonization, the strength of environmental influences (i.e., horizontal transmission), and potentially the homeostatic function of the niche microbiome.

2 citations

Journal ArticleDOI
TL;DR: The results suggest that Rahnella sp.
Abstract: Rahnella sp. ChDrAdgB13 is a dominant member of the gut bacterial core of species of the genus Dendroctonus, which is one of the most destructive pine forest bark beetles. The objectives of this study were identified in Rahnella sp. ChDrAdgB13 genome the glycosyl hydrolase families involved in carbohydrate metabolism and specifically, the genes that participate in xylan hydrolysis, to determine the functionality of a putative endo-1,4-β-D-xylanase, which results to be bifunctional xylanase–ferulic acid esterase called R13 Fae and characterize it biochemically. The carbohydrate-active enzyme prediction revealed 25 glycoside hydrolases, 20 glycosyl transferases, carbohydrate esterases, two auxiliary activities, one polysaccharide lyase, and one carbohydrate-binding module (CBM). The R13 Fae predicted showed high identity to the putative esterases and glycosyl hydrolases from Rahnella species and some members of the Yersiniaceae family. The r13 fae gene encodes 393 amino acids (43.5 kDa), containing a signal peptide, esterase catalytic domain, and CBM48. The R13 Fae modeling showed a higher binding affinity to ferulic acid, α-naphthyl acetate, and arabinoxylan, and a low affinity to starch. The R13 Fae recombinant protein showed activity on α-naphthyl acetate and xylan, but not on starch. This enzyme showed mesophilic characteristics, displaying its optimal activity at pH 6.0 and 25°C. The enzyme was stable at pH from 4.5 to 9.0, retaining nearly 66–71% of its original activity. The half-life of the enzyme was 23 days at 25°C. The enzyme was stable in the presence of metallic ions, except for Hg2+. The products of R13 Fae mediated hydrolysis of beechwood xylan were xylobiose and xylose, manifesting an exo-activity. The results suggest that Rahnella sp. ChDrAdgB13 hydrolyze xylan and its products could be assimilated by its host and other gut microbes as a nutritional source, demonstrating their functional role in the bacterial-insect interaction contributing to their fitness, development, and survival.

2 citations

References
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Journal ArticleDOI
TL;DR: The basic biology of Wolbachia is reviewed, with emphasis on recent advances in the authors' understanding of these fascinating endosymbionts, which are found in arthropods and nematodes.
Abstract: Wolbachia are common intracellular bacteria that are found in arthropods and nematodes. These alphaproteobacteria endosymbionts are transmitted vertically through host eggs and alter host biology in diverse ways, including the induction of reproductive manipulations, such as feminization, parthenogenesis, male killing and sperm-egg incompatibility. They can also move horizontally across species boundaries, resulting in a widespread and global distribution in diverse invertebrate hosts. Here, we review the basic biology of Wolbachia, with emphasis on recent advances in our understanding of these fascinating endosymbionts.

2,333 citations

Journal ArticleDOI
TL;DR: Recent technological and intellectual advances that have changed thinking about five questions about how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; and how is homeostasis maintained between animals and their symbionts are highlighted.
Abstract: In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal–bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal–bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.

2,103 citations


"Transmission efficiency drives host..." refers background or result in this paper

  • ...Surprisingly, our results also suggested that the relative fitness of host carriers versus non-carriers was less important for increasing host–microbe carriers than the existence of efficient microbial transmission [1]....

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  • ...Microbial symbionts can play crucial roles in many aspects of an organism’s biology [1] and associations between hosts andmicrobes can vary from commensal and parasitic relationships, through to obligate mutualisms inwhich the fate ofmicrobe and host are intimately entwined [2]....

    [...]

Journal ArticleDOI
TL;DR: Gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication, and the extent of these roles is still unclear and awaits further studies.
Abstract: Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies.

1,633 citations


"Transmission efficiency drives host..." refers background in this paper

  • ...by host diet selection [17,18], screening [5,19–21], gut physiology [22] or by spatial compartmentalization of microbial species within the gut [10]....

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  • ...In general, we expect environmental acquisition or HT to be less efficient than VT, lowering the likelihood that host–microbe associations will evolve [5,10,32,33]....

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  • ...Maternal inheritance is not restricted to intracellular symbionts, and there are increasing reports of symbiotic gut bacteria being transmitted from mother to offspring [10,11]....

    [...]

  • ...Host-led control of colonization could also be influenced by the morphological and physio-chemical conditions in the host gut [10]....

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Journal ArticleDOI
16 Sep 2016-Science
TL;DR: It is found that environmental conditions strongly influence the distribution of functional groups in marine microbial communities by shaping metabolic niches, but only weakly influence taxonomic composition within individual functional groups.
Abstract: Microbial metabolism powers biogeochemical cycling in Earth’s ecosystems. The taxonomic composition of microbial communities varies substantially between environments, but the ecological causes of this variation remain largely unknown. We analyzed taxonomic and functional community profiles to determine the factors that shape marine bacterial and archaeal communities across the global ocean. By classifying >30,000 marine microorganisms into metabolic functional groups, we were able to disentangle functional from taxonomic community variation. We find that environmental conditions strongly influence the distribution of functional groups in marine microbial communities by shaping metabolic niches, but only weakly influence taxonomic composition within individual functional groups. Hence, functional structure and composition within functional groups constitute complementary and roughly independent “axes of variation” shaped by markedly different processes.

1,566 citations


"Transmission efficiency drives host..." refers background in this paper

  • ...Host-led selection, in particular, is thought to promote parallelism/phylosymbiosis at a functional, but not necessarily taxonomic, level [50,51]....

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Journal ArticleDOI
TL;DR: Insect heritable symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.
Abstract: Insect heritable symbionts have proven to be ubiquitous, based on molecular screening of various insect lineages. Recently, molecular and experimental approaches have yielded an immensely richer understanding of their diverse biological roles, resulting in a burgeoning research literature. Increasingly, commonalities and intermediates are being discovered between categories of symbionts once considered distinct: obligate mutualists that provision nutrients, facultative mutualists that provide protection against enemies or stress, and symbionts such as Wolbachia that manipulate reproductive systems. Among the most farreaching impacts of widespread heritable symbiosis is that it may promote speciation by increasing reproductive and ecological isolation of host populations, and it effectively provides a means for transfer of genetic information among host lineages. In addition, insect symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.

1,438 citations


"Transmission efficiency drives host..." refers background in this paper

  • ...The lack of specialism and relaxed ecological constraints requiredmaymake this a frequent mechanism for symbiotic transmission [2,14,70]....

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  • ...Many insects carry heritable microbes [2,6,7] including the widespread intracellular symbionts Rickettsia, Cardinium and Wolbachia....

    [...]

  • ...The high fidelity of VT has facilitated the transition of many heritable symbionts to obligate associations, leading to the loss of their ability to propagate independently [2]....

    [...]

  • ...Microbial symbionts can play crucial roles in many aspects of an organism’s biology [1] and associations between hosts andmicrobes can vary from commensal and parasitic relationships, through to obligate mutualisms inwhich the fate ofmicrobe and host are intimately entwined [2]....

    [...]