Biology:Vertical transmission

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Short description: Transmission of a symbiont from parent to offspring

Vertical transmission of symbionts is the transfer of a microbial symbiont from the parent directly to the offspring.[1]  Many metazoan species carry symbiotic bacteria which play a mutualistic, commensal, or parasitic role.[1]  A symbiont is acquired by a host via horizontal, vertical, or mixed transmission.[2]

Fitness benefits

Vertical transmission, passage of symbiotic microflora from parents to offspring, is common in species of animals which have parental care. There are fitness benefits in providing youths with established microorganism community early on.[3]

  1. Immune system development: parents microbes prime young immune system.
  2. Disease resistance: because skin is already colonized by parental microbes, pathogen flora has a harder time to establish itself.
  3. Digestive help: parental microbes might help with digestion, as a result, the young ones can survive on a diet which would not meet their nutritious needs otherwise.
  4. Environmental adaptation: microflora might help to cope with environmental stress.
  5. Increased social cohesion: the microbiome may produce neurological or chemical signals that alter social behavior.[4]

Evolutionary consequences

Complex interdependence occurs between host and symbiont.[5] The genetic pool of the symbiont is generally smaller and more subject to genetic drift.[6] In true vertical transmission, the evolutionary outcomes of the host and symbiont are linked.[7] If there is mixed transmission, new genetic material may be introduced.[8] Generally, symbionts settle into specific niches and can even transfer part of their genome into the host nucleus.

Benefits

The mechanism promotes tightly coupled evolutionary pressure, which causes the host and symbiont to function as a holobiont.[9]

Disadvantages

Evolutionary bottlenecks lead to less symbiont diversity, and thus resilience.  Similarly, this greatly reduces the effective population size. Ultimately, without an influx of new genetic material, the population becomes clonal.  Mutations tend to persist in symbionts and build up over time.[10]

Transmission modes

Matrilineal

Germline

Since the egg contributes the organelles and has more space and opportunity for intracellular symbionts to be passed to subsequent generations, it is a very common method of vertical transmission.[1]  Intracellular symbionts can migrate from the bacteriocyte to the ovaries and become incorporated in germ cells.[11]

In plants, vertical transmission of microbial endophytes through germline can occur matrilineally via seed.[12] There are several mechanisms by which a seed can matrilineally become infected with endophytes. The mother plant can produce vascular connections from its somatic microbiomes to the endosperm.[12] Alternatively, endophytes can be transmitted directly when reproductive organs are developing in the shoot apical meristem.[12]

Live birth

Human infants acquire their microbiome from their mothers, from every sphere where there is contact.  This includes potentially the mother's vagina, gastrointestinal tract, skin, mouth and breastmilk.[13] These routes are typical if the delivery is a vaginal birth and the infant is nursed. When other actions, such as Caesarian delivery, bottle feeding, or maternal antibiotics during nursing occur, these modes of vertical transmission are disrupted.[14][15]

Human infants are generally protected from most viruses, bacteria and other pathogens while in the uterus as the placenta forms a barrier[16]. However, some viruses (e.g. Zika[17]) and bacteria (e.g. listeria[18]) can still pass through the placenta to the fetus through vertical transmission, which is why some foods are recommended to be avoided during pregnancy.

Patrilineal

Though extremely rare, Rickettsia is transmitted to Nephotettix cincticep through the paternal line in the sperm.[19]

In plants, vertical transmission of microbial endophytes through germline can occur patrilineally via pollen.[12] Patrilineal transmission has been hypothesized to be a common mechanism for fungal endophyte transmission,[12] as well as bacteria.[20]

Parental care

Microbes can be transmitted through the actions of parents caring for their offspring, such as the cultivation of gut microbes through regurgitation feeding.[21] This type of vertical transmission does not always occur via the behavior of the genetic parent; instead, other members of a social or family groups may transmit the microbial community, resulting in kin selection.[4][22]

Aposymbiotic

Earthworms (Eisenia) have an extracellular symbiont, Verminephrobacter. Rather than being passed through the egg in the germline, the young are aposymbiotic when still in the egg capsule; however, they acquire Verminephrobacter before the egg capsule ruptures, so it is still vertical transmission.[23]

Examples

Invertebrates

Vertical transmission of endosymbiotic bacteria is very common in insects.[24]

Wolbachia

It's estimated that about 70% of all insects carry the bacteria Wolbachia, which can be transmitted vertically as well as horizontally.[25] Depending on the host species, it may function as mutualist or a pathogen.[26] In order to maintain the infection within a host species, it must enter the forming egg cell and be transmitted through the germline. To improve the rate of vertical transmission, Wolbachia can alter its host's reproductive system[26] in a diverse array of mechanisms, such as induced parthenogenesis, male killing, or feminization.[27] All of these increase the ratio of infected females, which is beneficial to a matrilineally-spread infection.

Pea aphids and Buchnera

Pea Aphids do not get all of the necessary amino acids from their diet. Their obligate symbiont, Buchnera, synthesize the remainder.[11] [28]

Head lice and Candidatus Riesia pediculicola

The head louse (Pediculus humanus)  has an obligate symbiotic relationship with Candidatus Riesia pediculicola.  The louse provides shelter and protection while bacteria provides essential B vitamins. C. riesia lives in the bacteriocyte but move to the ovaries to be transmitted to the next generation.[29][30]

Tsetse flies and Wigglesworthia glossinidia

Tsetse flies have a fascinating life cycle. Tsetse gives life birth, which is extremely rare among insects. The fly fertilized one egg at the time and for the first three larval stages the single offspring developed inside the mother's uterus feeding on milk substance coming from milk glands in the uterus.[31][32][33][34] Through the "milk" the youngsters receive parent microflora including Wigglesworthia glossinidia, the bacteria providing host with vitamins B scarce in the tsetse fly's blood-only diet.[35][36]

Social spiders

Social spiders Stegodyphus dumicola live in Namibia and Botswana. The majority of females in the colony are virgins but participate in offspring care for reproducing females.[37] Offspring hatch symbiont-free, and bacterial symbionts are transmitted vertically across generations by social interactions with the onset of regurgitation feeding by (foster) mothers early in the development.[22]

Vertebrates

Caecililans

Caecilians feed youngsters by mother skin, passing to them the microflora which colonize youngster's skin and gut.[38] The mother's skin is adapted for this purpose, thickening beforehand and regenerating quickly after being consumed to continue providing for her young. She repeats the process several times during early development without significant harm to herself. The repeated nature of skin feeding means that juveniles are exposed to their mother microbiome several times, enhancing the likelihood of microbial gut and skin successful colonization.

Bornean foam‑nesting frogs

Bornean foam‑nesting frogs Leptomantis harrissoni tadpoles receive microbes from both their parents (vertically) and environment (horizontally).[3] Initially they have microbiomes resembling their parents and the exterior of the foam nest, but after one week in the pond tadpoles pick up new microbes from the pond environment.

Imitator dart frog

A Ranitomeya imitator dart frog feeds tadpoles with unfertilized trophic eggs. Anaerobic parabasalian protists are passed to the tadpoles via vertical transmission. In the gut, these protists express digestive enzymes Proteinases.[39] By doing so, they help youngsters to have the ability to digest fat and protein in the mother egg versus plant debris in the mini pond they live in. Genes that code for Proteinases are not present in the Ranitomeya genome. The symbiosis allows Ranitpomeya imitator to expand into the new ecological niche and tadpoles to grow more robustly.[39] Another mechanism of vertical transmission via parental care occurs when the father carries a tadpole on its back from the egg to the breeding pool, which allows the tadpole an opportunity to receive microflora patrilinealy.[40]

References

  1. ↑ 1.0 1.1 1.2 "A complex journey: transmission of microbial symbionts". Nature Reviews. Microbiology 8 (3): 218–230. March 2010. doi:10.1038/nrmicro2262. PMID 20157340. 
  2. ↑ "Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage". Environmental Microbiology 15 (7): 2073–2081. July 2013. doi:10.1111/1462-2920.12121. PMID 23574391. Bibcode: 2013EnvMi..15.2073K. 
  3. ↑ 3.0 3.1 "Early life skin microbial trajectory as a function of vertical and environmental transmission in Bornean foam-nesting frogs". Animal Microbiome 3 (1). December 2021. doi:10.1186/s42523-021-00147-8. PMID 34930504. 
  4. ↑ 4.0 4.1 Archie, Elizabeth A; Tung, Jenny (2015-12-01). "Social behavior and the microbiome". Current Opinion in Behavioral Sciences. The integrative study of animal behavior 6: 28–34. doi:10.1016/j.cobeha.2015.07.008. ISSN 2352-1546. 
  5. ↑ "Rickettsia as obligate and mycetomic bacteria". FASEB Journal 20 (13): 2372–2374. November 2006. doi:10.1096/fj.06-5870fje. PMID 17012243. 
  6. ↑ "Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes". Molecular Biology and Evolution 16 (1): 83–97. January 1999. doi:10.1093/oxfordjournals.molbev.a026040. PMID 10331254. 
  7. ↑ "Interactions between vertically transmitted symbionts: cooperation or conflict?". Trends in Microbiology 17 (3): 95–99. March 2009. doi:10.1016/j.tim.2008.12.002. PMID 19230673. 
  8. ↑ "Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral". Heredity 121 (6): 524–536. December 2018. doi:10.1038/s41437-018-0059-0. PMID 29453423. Bibcode: 2018Hered.121..524Q. 
  9. ↑ "What is the hologenome concept of evolution?". F1000Research 7: 1664. 2018-10-19. doi:10.12688/f1000research.14385.1. PMID 30410727. 
  10. ↑ "Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis". Nature Reviews. Microbiology 4 (9): 670–681. September 2006. doi:10.1038/nrmicro1472. PMID 16912712. 
  11. ↑ 11.0 11.1 "Bacteriocyte cell death in the pea aphid/Buchnera symbiotic system". Proceedings of the National Academy of Sciences of the United States of America 115 (8): E1819–E1828. February 2018. doi:10.1073/pnas.1720237115. PMID 29432146. Bibcode: 2018PNAS..115E1819S. 
  12. ↑ 12.0 12.1 12.2 12.3 12.4 Frank, Anna Carolin; Saldierna Guzmán, Jessica Paola; Shay, Jackie E. (December 2017). "Transmission of Bacterial Endophytes" (in en). Microorganisms 5 (4): 70. doi:10.3390/microorganisms5040070. ISSN 2076-2607. PMID 29125552. 
  13. ↑ "Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life". Cell Host & Microbe 17 (5): 690–703. May 2015. doi:10.1016/j.chom.2015.04.004. PMID 25974306. 
  14. ↑ "Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences". Cell 158 (4): 705–721. August 2014. doi:10.1016/j.cell.2014.05.052. PMID 25126780. 
  15. ↑ "Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns". Proceedings of the National Academy of Sciences of the United States of America 107 (26): 11971–11975. June 2010. doi:10.1073/pnas.1002601107. PMID 20566857. Bibcode: 2010PNAS..10711971D. 
  16. ↑ Arthurs, Anya Lara; Jankovic-Karasoulos, Tanja; Roberts, Claire Trelford (2021-12-01). "COVID-19 in pregnancy: What we know from the first year of the pandemic". Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 1867 (12). doi:10.1016/j.bbadis.2021.166248. ISSN 0925-4439. PMID 34461257. 
  17. ↑ Ades, A E; Soriano-Arandes, Antoni; Alarcon, Ana; Bonfante, Francesco; Thorne, Claire; Peckham, Catherine S; Giaquinto, Carlo (2021-04-01). "Vertical transmission of Zika virus and its outcomes: a Bayesian synthesis of prospective studies". The Lancet Infectious Diseases 21 (4): 537–545. doi:10.1016/S1473-3099(20)30432-1. ISSN 1473-3099. PMC 7992034. https://www.sciencedirect.com/science/article/pii/S1473309920304321. 
  18. ↑ Lamond, Nicole M.; Freitag, Nancy E. (2018-05-25). "Vertical Transmission of Listeria monocytogenes: Probing the Balance between Protection from Pathogens and Fetal Tolerance". Pathogens (Basel, Switzerland) 7 (2): 52. doi:10.3390/pathogens7020052. ISSN 2076-0817. PMID 29799503. 
  19. ↑ "Intrasperm vertical symbiont transmission". Proceedings of the National Academy of Sciences of the United States of America 111 (20): 7433–7437. May 2014. doi:10.1073/pnas.1402476111. PMID 24799707. Bibcode: 2014PNAS..111.7433W. 
  20. ↑ Hodgson, Susan; de Cates, Catherine; Hodgson, Joshua; Morley, Neil J.; Sutton, Brian C.; Gange, Alan C. (April 2014). "Vertical transmission of fungal endophytes is widespread in forbs" (in en). Ecology and Evolution 4 (8): 1199–1208. doi:10.1002/ece3.953. ISSN 2045-7758. PMID 24834319. Bibcode: 2014EcoEv...4.1199H. 
  21. ↑ Miller, Christopher James; Bates, Scott Thomas; Gielda, Lindsay M.; Creighton, J. Curtis (2019-12-02). "Examining transmission of gut bacteria to preserved carcass via anal secretions in Nicrophorus defodiens" (in en). PLOS ONE 14 (12). doi:10.1371/journal.pone.0225711. ISSN 1932-6203. PMID 31790470. Bibcode: 2019PLoSO..1425711M. 
  22. ↑ 22.0 22.1 "Social transmission of bacterial symbionts homogenizes the microbiome within and across generations of group-living spiders". ISME Communications 3 (1). June 2023. doi:10.1038/s43705-023-00256-2. PMID 37330540. Bibcode: 2023ISMEC...3...60R. 
  23. ↑ "Transmission of nephridial bacteria of the earthworm Eisenia fetida". Applied and Environmental Microbiology 72 (1): 769–775. January 2006. doi:10.1128/AEM.72.1.769-775.2006. PMID 16391117. Bibcode: 2006ApEnM..72..769D. 
  24. ↑ "Bacterial symbionts in insects or the story of communities affecting communities". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 366 (1569): 1389–1400. May 2011. doi:10.1098/rstb.2010.0226. PMID 21444313. 
  25. ↑ "Wolbachia infection in native populations of Blattella germanica and Periplaneta americana". PLOS ONE 18 (4). 2023-04-20. doi:10.1371/journal.pone.0284704. PMID 37079598. Bibcode: 2023PLoSO..1884704C. 
  26. ↑ 26.0 26.1 Correa, Claudia C.; Ballard, J. W. O. (2016). "Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator". Frontiers in Ecology and Evolution 3: 153. doi:10.3389/fevo.2015.00153. ISSN 2296-701X. Bibcode: 2016FrEEv...3..153C. 
  27. ↑ Vavre, Fabrice; Mouton, Laurence; Pannebakker, Bart A. (2009-01-01), "Chapter 12 Drosophila–Parasitoid Communities as Model Systems for Host–Wolbachia Interactions", Advances in Parasitology Volume 70, 70, Academic Press, pp. 299–331, doi:10.1016/s0065-308x(09)70012-0, ISBN 978-0-12-374792-1, PMID 19773076, https://www.sciencedirect.com/science/article/pii/S0065308X09700120, retrieved 2024-05-06 
  28. ↑ "Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera". Annual Review of Entomology 43 (1): 17–37. January 1998. doi:10.1146/annurev.ento.43.1.17. PMID 15012383. 
  29. ↑ "Symbiotic bacteria associated with stomach discs of human lice". Applied and Environmental Microbiology 72 (11): 7349–7352. November 2006. doi:10.1128/AEM.01429-06. PMID 16950915. Bibcode: 2006ApEnM..72.7349S. 
  30. ↑ Human DNA Extracted From Nits on Ancient Mummies Sheds Light on South American Ancestry . SciTechDaily, December 28, 2021. Source: University of Reading.
  31. ↑ "Adenotrophic viviparity in tsetse flies: potential for population control and as an insect model for lactation". Annual Review of Entomology 60 (1): 351–371. January 2015. doi:10.1146/annurev-ento-010814-020834. PMID 25341093. 
  32. ↑ "Physiology of tsetse flies (Glossina spp.) (Diptera: Glossinidae): a review" (in en). Bulletin of Entomological Research 67 (4): 523–574. December 1977. doi:10.1017/S0007485300006933. ISSN 1475-2670. https://www.cambridge.org/core/journals/bulletin-of-entomological-research/article/abs/physiology-of-tsetse-flies-glossina-spp-diptera-glossinidae-a-review/21A12EB47CF87E7CF8E17A13131320D8. 
  33. ↑ "Dynamics of the pregnancy cycle in the tsetse Glossina morsitans". Journal of Insect Physiology 20 (6): 1015–1026. June 1974. doi:10.1016/0022-1910(74)90143-7. PMID 4839338. Bibcode: 1974JInsP..20.1015D. 
  34. ↑ "Interpreting Morphological Adaptations Associated with Viviparity in the Tsetse Fly Glossina morsitans (Westwood) by Three-Dimensional Analysis". Insects 11 (10): 651. September 2020. doi:10.3390/insects11100651. PMID 32977418. 
  35. ↑ "Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies". International Journal of Systematic Bacteriology 45 (4): 848–851. October 1995. doi:10.1099/00207713-45-4-848. PMID 7547309. 
  36. ↑ "Microbe Profile: Wigglesworthia glossinidia: the tsetse fly's significant other". Microbiology 168 (9). September 2022. doi:10.1099/mic.0.001242. PMID 36129743. 
  37. ↑ "Extreme allomaternal care and unequal task participation by unmated females in a cooperatively breeding spider" (in en). Animal Behaviour 132: 101–107. October 2017. doi:10.1016/j.anbehav.2017.08.006. https://linkinghub.elsevier.com/retrieve/pii/S0003347217302555. 
  38. ↑ "Parental care contributes to vertical transmission of microbes in a skin-feeding and direct-developing caecilian". Animal Microbiome 5 (1). May 2023. doi:10.1186/s42523-023-00243-x. PMID 37189209. 
  39. ↑ 39.0 39.1 Weinfurther, K. D.; Stuckert, A. M. M.; Muscarella, M. E.; Peralta, A. L.; Summers, K. (June 2023). "Evidence for a Parabasalian Gut Symbiote in Egg-Feeding Poison Frog Tadpoles in Peru" (in en). Evolutionary Biology 50 (2): 239–248. doi:10.1007/s11692-023-09602-7. ISSN 0071-3260. Bibcode: 2023EvBio..50..239W. 
  40. ↑ Macedo, Regina H., ed (2014). Sexual selection: perspectives and models from the Neotropics. Amsterdam ; Boston: Elsevier, AP. ISBN 978-0-12-416028-6. OCLC 854749429. 



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