Initial acquisition of microbiota

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The initial acquisition of microbiota is the formation of an organism's microbiota immediately before and after birth. The microbiota (also called flora) are all the microorganisms including bacteria, archaea and fungi that colonize the organism. The microbiome is another term for microbiota or can refer to the collected genomes.

Contents

Many of these microorganisms interact with the host in ways that are beneficial and often play an integral role in processes like digestion and immunity. [1] The microbiome is dynamic: it varies between individuals, over time, and can influenced by both endogenous and exogenous forces. [2]

Abundant research in invertebrates [3] [4] [5] has shown that endosymbionts may be transmitted vertically to oocytes or externally transmitted during oviposition. [6] Research on the acquisition of microbial communities in vertebrates is relatively sparse, but also suggests that vertical transmission may occur. [7] [8]

In humans

Early hypotheses assumed that human babies are born sterile and that any bacterial presence in the uterus would be harmful to the fetus. [7] Some believed that both the womb and maternal milk were sterile, and that bacteria did not enter an infant's intestinal tract until supplementary food was provided. [9] In 1900, the French pediatrician Henry Tissier isolated Bifidobacterium from the stool of healthy, breast-fed infants. [10] [11] He concluded that breast milk was not sterile and suggested that diarrhea caused by an imbalance of intestinal flora could be treated by supplementing food with Bifidobacterium. [12] However, Tissier still claimed that the womb was sterile and that infants did not come into contact with bacteria until entering the birth canal. [11]

Over the last few decades, research on the perinatal acquisition of microbiota in humans has expanded as a result of developments in DNA sequencing technology. [7] Bacteria have been detected in umbilical cord blood, [13] amniotic fluid, [14] and fetal membranes [15] of healthy, term babies. The meconium, an infant's first bowel movement of digested amniotic fluid, has also been shown to contain a diverse community of microbes. [13] These microbial communities consist of genera commonly found in the mouth and intestines, which may be transmitted to the uterus via the blood stream, and in the vagina, which may ascend through the cervix. [7] [13]

In non-human vertebrates

In one experiment, pregnant mice were given food containing genetically labeled Enterococcus faecium. [16] The meconium of term offspring delivered by these mice via sterile C-section was found to contain labeled E. faecium, while pups from control mice given non-inoculated food did not contain E. faecium. This evidence supports the possibility of vertical microbial transmission in mammals.

Most research on vertical transmission in non-mammalian vertebrates focuses on pathogens in agricultural animals (e.g. chicken, fish). [7] [17] [18] It is not known whether these species also incorporate commensal flora into eggs.

In invertebrates

Marine sponges are host to many sponge-specific microbe species that are found across several sponge lineages. [19] These microbes are detected in divergent populations without overlapping ranges but are not found in the sponges' immediate environment. As a result, it is thought that the symbionts were established by a colonization event before sponges diversified and are maintained through vertical (and, to a lesser extent, horizontal) transmission. [20] The presence of microorganisms in both the oocytes and in the embryos of sponges has been confirmed. [20] [21]

Many insects depend on microbial symbionts to obtain amino acids and other nutrients that are not available from their primary food source. [7] Microbiota may be passed on to offspring via bacteriocytes associated with the ovaries or developing embryo, [5] [22] [23] by feeding larvae with microbe-fortified food, [24] or by smearing eggs with a medium containing microbes during oviposition. [25] [26] Alternatively, in other instances, microbiota composition can also be determined by the environment, as is the case for mosquito larvae, living in the water. [27]

See also

Related Research Articles

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.

<span class="mw-page-title-main">Human microbiome</span> Microorganisms in or on human skin and biofluids

The human microbiome is the aggregate of all microbiota that reside on or within human tissues and biofluids along with the corresponding anatomical sites in which they reside, including the skin, mammary glands, seminal fluid, uterus, ovarian follicles, lung, saliva, oral mucosa, conjunctiva, biliary tract, and gastrointestinal tract. Types of human microbiota include bacteria, archaea, fungi, protists, and viruses. Though micro-animals can also live on the human body, they are typically excluded from this definition. In the context of genomics, the term human microbiome is sometimes used to refer to the collective genomes of resident microorganisms; however, the term human metagenome has the same meaning.

<span class="mw-page-title-main">Gut microbiota</span> Community of microorganisms in the gut

Gut microbiota, gut microbiome, or gut flora, are the microorganisms, including bacteria, archaea, fungi, and viruses, that live in the digestive tracts of animals. The gastrointestinal metagenome is the aggregate of all the genomes of the gut microbiota. The gut is the main location of the human microbiome. The gut microbiota has broad impacts, including effects on colonization, resistance to pathogens, maintaining the intestinal epithelium, metabolizing dietary and pharmaceutical compounds, controlling immune function, and even behavior through the gut–brain axis.

<i>Bacteroides</i> Genus of bacteria

Bacteroides is a genus of Gram-negative, obligate anaerobic bacteria. Bacteroides species are non endospore-forming bacilli, and may be either motile or nonmotile, depending on the species. The DNA base composition is 40–48% GC. Unusual in bacterial organisms, Bacteroides membranes contain sphingolipids. They also contain meso-diaminopimelic acid in their peptidoglycan layer.

Dysbiosis is characterized by a disruption to the microbiome resulting in an imbalance in the microbiota, changes in their functional composition and metabolic activities, or a shift in their local distribution. For example, a part of the human microbiota such as the skin flora, gut flora, or vaginal flora, can become deranged, with normally dominating species underrepresented and normally outcompeted or contained species increasing to fill the void. Dysbiosis is most commonly reported as a condition in the gastrointestinal tract.

<span class="mw-page-title-main">Oral microbiology</span>

Oral microbiology is the study of the microorganisms (microbiota) of the oral cavity and their interactions between oral microorganisms or with the host. The environment present in the human mouth is suited to the growth of characteristic microorganisms found there. It provides a source of water and nutrients, as well as a moderate temperature. Resident microbes of the mouth adhere to the teeth and gums to resist mechanical flushing from the mouth to stomach where acid-sensitive microbes are destroyed by hydrochloric acid.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, mutualistic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

<i>Bifidobacterium</i> Genus of bacteria

Bifidobacterium is a genus of gram-positive, nonmotile, often branched anaerobic bacteria. They are ubiquitous inhabitants of the gastrointestinal tract though strains have been isolated from the vagina and mouth of mammals, including humans. Bifidobacteria are one of the major genera of bacteria that make up the gastrointestinal tract microbiota in mammals. Some bifidobacteria are used as probiotics.

The hologenome theory of evolution recasts the individual animal or plant as a community or a "holobiont" – the host plus all of its symbiotic microbes. Consequently, the collective genomes of the holobiont form a "hologenome". Holobionts and hologenomes are structural entities that replace misnomers in the context of host-microbiota symbioses such as superorganism, organ, and metagenome. Variation in the hologenome may encode phenotypic plasticity of the holobiont and can be subject to evolutionary changes caused by selection and drift, if portions of the hologenome are transmitted between generations with reasonable fidelity. One of the important outcomes of recasting the individual as a holobiont subject to evolutionary forces is that genetic variation in the hologenome can be brought about by changes in the host genome and also by changes in the microbiome, including new acquisitions of microbes, horizontal gene transfers, and changes in microbial abundance within hosts. Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts. For recent literature on holobionts and hologenomes published in an open access platform, see the following reference.

<span class="mw-page-title-main">Microbiome</span> Microbial community assemblage and activity

A microbiome is the community of microorganisms that can usually be found living together in any given habitat. It was defined more precisely in 1988 by Whipps et al. as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity". In 2020, an international panel of experts published the outcome of their discussions on the definition of the microbiome. They proposed a definition of the microbiome based on a revival of the "compact, clear, and comprehensive description of the term" as originally provided by Whipps et al., but supplemented with two explanatory paragraphs. The first explanatory paragraph pronounces the dynamic character of the microbiome, and the second explanatory paragraph clearly separates the term microbiota from the term microbiome.

The microbiota are the sum of all symbiotic microorganisms living on or in an organism. The fruit fly Drosophila melanogaster is a model organism and known as one of the most investigated organisms worldwide. The microbiota in flies is less complex than that found in humans. It still has an influence on the fitness of the fly, and it affects different life-history characteristics such as lifespan, resistance against pathogens (immunity) and metabolic processes (digestion). Considering the comprehensive toolkit available for research in Drosophila, analysis of its microbiome could enhance our understanding of similar processes in other types of host-microbiota interactions, including those involving humans. Microbiota plays key roles in the intestinal immune and metabolic responses via their fermentation product, acetate.

The Human Microbiome Project (HMP), completed in 2012, laid the foundation for further investigation into the role the microbiome plays in overall health and disease. One area of particular interest is the role which delivery mode plays in the development of the infant/neonate microbiome and what potential implications this may have long term. It has been found that infants born via vaginal delivery have microbiomes closely mirroring that of the mother's vaginal microbiome, whereas those born via cesarean section tend to resemble that of the mother's skin. One notable study from 2010 illustrated an abundance of Lactobacillus and other typical vaginal genera in stool samples of infants born via vaginal delivery and an abundance of Staphylococcus and Corynebacterium, commonly found on the skin surfaces, in stool samples of infants born via cesarean section. From these discoveries came the concept of vaginal seeding, also known as microbirthing, which is a procedure whereby vaginal fluids are applied to a new-born child delivered by caesarean section. The idea of vaginal seeding was explored in 2015 after Maria Gloria Dominguez-Bello discovered that birth by caesarean section significantly altered the newborn child's microbiome compared to that of natural birth. The purpose of the technique is to recreate the natural transfer of bacteria that the baby gets during a vaginal birth. It involves placing swabs in the mother's vagina, and then wiping them onto the baby's face, mouth, eyes and skin. Due to the long-drawn nature of studying the impact of vaginal seeding, there are a limited number of studies available that support or refute its use. The evidence suggests that applying microbes from the mother's vaginal canal to the baby after cesarean section may aid in the partial restoration of the infant's natural gut microbiome with an increased likelihood of pathogenic infection to the child via vertical transmission.

<span class="mw-page-title-main">Holobiont</span> Host and associated species living as a discrete ecological unit

A holobiont is an assemblage of a host and the many other species living in or around it, which together form a discrete ecological unit through symbiosis, though there is controversy over this discreteness. The components of a holobiont are individual species or bionts, while the combined genome of all bionts is the hologenome. The holobiont concept was initially introduced by the German theoretical biologist Adolf Meyer-Abich in 1943, and then apparently independently by Dr. Lynn Margulis in her 1991 book Symbiosis as a Source of Evolutionary Innovation. The concept has evolved since the original formulations. Holobionts include the host, virome, microbiome, and any other organisms which contribute in some way to the functioning of the whole. Well-studied holobionts include reef-building corals and humans.

<span class="mw-page-title-main">Placental microbiome</span>

The placental microbiome is the nonpathogenic, commensal bacteria claimed to be present in a healthy human placenta and is distinct from bacteria that cause infection and preterm birth in chorioamnionitis. Until recently, the healthy placenta was considered to be a sterile organ but now genera and species have been identified that reside in the basal layer.

Hologenomics is the omics study of hologenomes. A hologenome is the whole set of genomes of a holobiont, an organism together with all co-habitating microbes, other life forms, and viruses. While the term hologenome originated from the hologenome theory of evolution, which postulates that natural selection occurs on the holobiont level, hologenomics uses an integrative framework to investigate interactions between the host and its associated species. Examples include gut microbe or viral genomes linked to human or animal genomes for host-microbe interaction research. Hologenomics approaches have also been used to explain genetic diversity in the microbial communities of marine sponges.

<span class="mw-page-title-main">Pharmacomicrobiomics</span>

Pharmacomicrobiomics, proposed by Prof. Marco Candela for the ERC-2009-StG project call, and publicly coined for the first time in 2010 by Rizkallah et al., is defined as the effect of microbiome variations on drug disposition, action, and toxicity. Pharmacomicrobiomics is concerned with the interaction between xenobiotics, or foreign compounds, and the gut microbiome. It is estimated that over 100 trillion prokaryotes representing more than 1000 species reside in the gut. Within the gut, microbes help modulate developmental, immunological and nutrition host functions. The aggregate genome of microbes extends the metabolic capabilities of humans, allowing them to capture nutrients from diverse sources. Namely, through the secretion of enzymes that assist in the metabolism of chemicals foreign to the body, modification of liver and intestinal enzymes, and modulation of the expression of human metabolic genes, microbes can significantly impact the ingestion of xenobiotics.

Vertical transmission of symbionts is the transfer of a microbial symbiont from the parent directly to the offspring. Many metazoan species carry symbiotic bacteria which play a mutualistic, commensal, or parasitic role. A symbiont is acquired by a host via horizontal, vertical, or mixed transmission.

<span class="mw-page-title-main">Marine microbiome</span>

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.

<span class="mw-page-title-main">Plant microbiome</span>

The plant microbiome, also known as the phytomicrobiome, plays roles in plant health and productivity and has received significant attention in recent years. The microbiome has been defined as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity".

<span class="mw-page-title-main">Marine holobiont</span>

The holobiont concept is a renewed paradigm in biology that can help to describe and understand complex systems, like the host-microbe interactions that play crucial roles in marine ecosystems. However, there is still little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them and their ecological consequences. The holobiont concept posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution.

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