|Image credit to Robert M. Brucker|
In this new paper in PLOS Biology, PhD student and NSF graduate research fellow Lisa Funkhouser (@DNAdiva87) and I propose that the existing evidence from disparate study systems and diverse subdisciplines compels a substantial phase of study on the ubiquity of maternal microbial transmission in animals, and it has critical implications for health, evolution and the hologenome concept.
The term “maternal transmission” has traditionally referred to strict vertical transmission of a microbial symbiont from mother to offspring in invertebrates, usually through the incorporation of symbionts into developing oocytes or embryos. It is likely viewed in this context due to the pioneering work of Paul Buchner, whose seminal book Endosymbiosis of Animals with Plant Microorganisms dissects in exquisite detail symbiont transfer in an expansive range of invertebrates, especially insects. For a nice summary of Buchner, see Prof. Jan Sapp's 2002 paper on him. Since the English publication of Buchner’s work in 1965, elegant studies in insect models have further emphasized the importance of maternal transmission in maintaining obligate mutualistic relationships in invertebrates (see this 2006 primer on the topic from Nancy Moran).
Conversely, in humans, “mother-to-child” transmission is commonly used in a negative context to describe the transfer of a pathogen, parasite or virus from an infected mother to her infant. However, current interest in the human microbiome has refocused attention on the transfer of commensal and beneficial bacteria from mother to child. Importantly, increasing evidence indicates that valuable maternal microbes are transferred before, during, and after birth to vaginally-delivered, breast-fed infants, while disruption of natural maternal transfer through Cesarean sections and formula-feeding puts children at significantly higher risk for immune-mediated diseases, such as asthma, celiac disease, and inflammatory bowel disease, as well as for childhood obesity.
In this paper, Lisa and I explore the emergent paradigm that maternal microbial transmission in animals is a universal phenomenon that ensures transgenerational maintenance of important host-microbe partnerships or functions over evolutionary time scales. To our knowledge, ours is the first literature review to encompass all forms of maternal transmission across the animal kingdom. Some of the stories we scavenged from the literature surprised even us. Thus, we have classified maternal transmission into two broad categories that reflect route of transmission (internal versus external) in order to facilitate future discussion of maternal transmission mechanisms in both invertebrates and vertebrates. We have defined internal maternal transmission as any transfer of microbes to an oocyte or embryo while still developing within the maternal body cavity, while external maternal transmission refers to the ingestion of maternal microbes after delivery, such as breastfeeding in humans or “egg smearing” in insects. As such, the content of this review
- Illustrates the universality of maternal symbiont transmission by highlighting diverse systems that maintain symbionts through maternal transmission
- Dissects the mechanisms by which maternal transmission is achieved in these systems
- Assesses sources of potential maternal transmission in humans and their effect on human health.