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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. [1] While the term hologenome originated from the hologenome theory of evolution, which postulates that natural selection occurs on the holobiont level, [2] hologenomics uses an integrative framework to investigate interactions between the host and its associated species. Examples include gut microbe [3] or viral [4] genomes linked to human or animal genomes for host-microbe interaction research. [5] Hologenomics approaches have also been used to explain genetic diversity in the microbial communities of marine sponges. [6]

History

The origins of hologenomics revolves around the hologenome theory of evolution, which describes individual multicellular organisms, microbes, and viruses establishing symbiotic relationships and undergoing coevolution together. [2] [7] Richard Jefferson introduced the term 'hologenome' to describe the host-symbiont genome as an evolutionary unit. [8] Prior to this, Lynn Margulis used the term 'holobiont' to describe hosts and their associated species as an ecological unit. [9]

Eukaryotes-prokaryotes coevolution

Distinct microbial communities in sponges converge to have common functionality despite retaining phylogenetic differences. [10]

Earliest evidence of multicellular-unicellular interactions are seen in sponges, which are a well studied hologenomic system. Porifera are often described as holobionts because they harbor a wide range of bacteria, archaea and algae. Microbial communities present have been observed in facilitating metabolic functions and immune responses. [10] Offspring inherit these microbial colonies via vertical and/or horizontal transmission. [10] Symbiont colonies are transferred through parental gametes in vertical transmission, whereas offspring acquire same colonies from their environment in horizontal transmission. Vertical transmission is also seen in terrestrial organisms like C. ocellatus, where gammaproteobacteria in the parental gut is vertically transferred through egg contamination. [11]

Criticism

The hologenome theory evolution is not fully accepted, and research in microbial-host phylogenetics is ongoing. Rather than the selection of corals with certain symbiotic microbial communities, coral bleaching may simply be a result of environmental stressors, and bacterial presence in bleached coral may be explained simply as opportunistic colonization. [12] Ubiquity testing also revealed many different bacterial and algal symbionts that are not associated with a single species of coral, [13] suggesting that hologenomics just identifies and validates mechanistic interactions between pathogens, microbes, and their hosts. [14]

Examples of discoveries with hologenomic approaches

  • Nanopore sequencing - Profiling organelle genomes in the holobiont C. ashmeadii revealed that Rhodospirillaceae was dominant among six putative endosymbionts. [15]
  • 16S rRNA sequencing - Sponge-specific microbial communities were profiled with rRNA and rRNA gene sequencing, providing insight into bacterial diversity and activity of those communities. [16]
  • Metagenomic DNA - Gene profiles of sponge microbiomes were compared to surrounding planktonic communities. [17] Core function genes of microbial symbionts expressed consistent patterns of phylogeny and function that differ from planktonic samples, demonstrating host-symbiont co-evolution. [17]

Applications

Medicine

It's hypothesized the continued incidence non-infectious diseases is a result of modernization reducing the diversity of symbiotic microbes. [14] The human microbiome has also been correlated to numerous etiologies of non-communicable disease, such as brain disorders, [18] cancer, [19] [20] and heart disease. [21] Interactions between human microbiome and human health are complex and suggest a hologenomic approach.

Disease biomarkers can be found by investigating lifestyle, genomic differences, and mRNA/ protein/ metabolite profiles of the patient and their microbiota. [14] For investigating microbiomes and specifically microbiota subcommunities that may contribute to a disease phenotype, longitudinal studies are recommended as everyone has a personalized microbiome with small differences in microbiome phylotypes. [14] A personalized plan managing a person’s microbiome can then be developed, with prebiotics nurturing beneficial endogenous microbes, and probiotics manipulating a person’s hologenome. [22]

Immunology

Conditional mutualism, where parasites have mutualistic effects under certain environmental/ecological conditions, have been found with holobiont-holobiont interactions. [23] Maturation of mammalian host immune systems has been known to involve gastrointestinal flora. [24] Understanding microorganism recognition of foreign pathogenic invasion and how host immunity favors the most ideal symbiont may aid in discovering novel therapeutic treatments to combat evolving diseases.

See also

References

  1. ^ Rosenberg, Eugene; Zilber-Rosenberg, Ilana (2018-04-25). "The hologenome concept of evolution after 10 years". Microbiome. 6 (1): 78. doi: 10.1186/s40168-018-0457-9. ISSN  2049-2618. PMC  5922317. PMID  29695294.
  2. ^ a b Number 6 in a series of 7 VHS recordings, A Decade of PCR: Celebrating 10 Years of Amplification, Cold Spring Harbor Laboratory Press, 1994. ISBN  0-87969-473-4.
  3. ^ Denman, Stuart E.; McSweeney, Christopher S. (2015-02-16). "The Early Impact of Genomics and Metagenomics on Ruminal Microbiology". Annual Review of Animal Biosciences. 3 (1): 447–465. doi: 10.1146/annurev-animal-022114-110705. ISSN  2165-8102. PMID  25387109.
  4. ^ Patowary, Ashok; Chauhan, Rajendra Kumar; Singh, Meghna; KV, Shamsudheen; Periwal, Vinita; KP, Kushwaha; Sapkal, Gajanand N.; Bondre, Vijay P.; Gore, Milind M. (2012-01-01). "De novo identification of viral pathogens from cell culture hologenomes". BMC Research Notes. 5: 11. doi: 10.1186/1756-0500-5-11. ISSN  1756-0500. PMC  3284880. PMID  22226071.
  5. ^ Miller, William B. Jr. (2013). The Microcosm Within: Evolution and Extinction in the Hologenome. Universal-Publishers. ISBN  978-1612332772.
  6. ^ Webster, Nicole S.; Thomas, Torsten (2016-05-04). "The Sponge Hologenome". mBio. 7 (2): e00135–16. doi: 10.1128/mBio.00135-16. ISSN  2150-7511. PMC  4850255. PMID  27103626.
  7. ^ Rosenberg, Eugene; Zilber-Rosenberg, Ilana (2018-04-25). "The hologenomce concept of evolution after 10 years". Microbiome. 6 (1): 78. doi: 10.1186/s40168-018-0457-9. ISSN  2049-2618. PMC  5922317. PMID  29695294.
  8. ^ Number 6 in a series of 7 VHS recordings, A Decade of PCR: Celebrating 10 Years of Amplification, Cold Spring Harbor Laboratory Press, 1994. ISBN  0-87969-473-4.
  9. ^ Margulis, University of Massachusetts Amherst Massachusetts Lynn; Margulis, Lynn; Fester, René (1991). Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis. MIT Press. ISBN  978-0-262-13269-5.
  10. ^ a b c Webster, Nicole S.; Thomas, Torsten (2016-05-04). "The Sponge Hologenome". mBio. 7 (2): e00135-16. doi: 10.1128/mBio.00135-16. ISSN  2150-7511. PMC  4850255. PMID  27103626.
  11. ^ Kaiwa, Nahomi; Hosokawa, Takahiro; Kikuchi, Yoshitomo; Nikoh, Naruo; Meng, Xian Ying; Kimura, Nobutada; Ito, Motomi; Fukatsu, Takema (2010-06-01). "Primary Gut Symbiont and Secondary, Sodalis-Allied Symbiont of the Scutellerid Stinkbug Cantao ocellatus". Applied and Environmental Microbiology. 76 (11): 3486–3494. Bibcode: 2010ApEnM..76.3486K. doi: 10.1128/AEM.00421-10. ISSN  0099-2240. PMC  2876435. PMID  20400564.
  12. ^ Ainsworth, T. D.; Fine, M.; Roff, G.; Hoegh-Guldberg, O. (2008). "Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica". The ISME Journal. 2 (1): 67–73. doi: 10.1038/ismej.2007.88. ISSN  1751-7362. PMID  18059488. S2CID  1032896.
  13. ^ Hester, Eric R.; Barott, Katie L.; Nulton, Jim; Vermeij, Mark JA; Rohwer, Forest L. (May 2016). "Stable and sporadic symbiotic communities of coral and algal holobionts". The ISME Journal. 10 (5): 1157–1169. doi: 10.1038/ismej.2015.190. ISSN  1751-7370. PMC  5029208. PMID  26555246.
  14. ^ a b c d Theis, Kevin R. (2018-04-10). "Hologenomics: Systems-Level Host Biology". mSystems. 3 (2). doi: 10.1128/mSystems.00164-17. ISSN  2379-5077. PMC  5895875. PMID  29657963.
  15. ^ Sauvage, Thomas; Schmidt, William E.; Yoon, Hwan Su; Paul, Valerie J.; Fredericq, Suzanne (2019-11-13). "Promising prospects of nanopore sequencing for algal hologenomics and structural variation discovery". BMC Genomics. 20 (1): 850. doi: 10.1186/s12864-019-6248-2. ISSN  1471-2164. PMC  6854639. PMID  31722669.
  16. ^ Kamke, Janine; Taylor, Michael W.; Schmitt, Susanne (2017-01-07). "Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons". The ISME Journal. 4 (4): 498–508. doi: 10.1038/ismej.2009.143. ISSN  1751-7370. PMID  20054355.
  17. ^ a b Fan, Lu; Reynolds, David; Liu, Michael; Stark, Manuel; Kjelleberg, Staffan; Webster, Nicole S.; Thomas, Torsten (2012-07-03). "Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts". Proceedings of the National Academy of Sciences. 109 (27): E1878–E1887. doi: 10.1073/pnas.1203287109. ISSN  0027-8424. PMC  3390844. PMID  22699508.
  18. ^ Zhu, Sibo; Jiang, Yanfeng; Xu, Kelin; Cui, Mei; Ye, Weimin; Zhao, Genming; Jin, Li; Chen, Xingdong (2020-01-17). "The progress of gut microbiome research related to brain disorders". Journal of Neuroinflammation. 17 (1): 25. doi: 10.1186/s12974-020-1705-z. ISSN  1742-2094. PMC  6969442. PMID  31952509.
  19. ^ Xavier, Joao B.; Young, Vincent B.; Skufca, Joseph; Ginty, Fiona; Testerman, Traci; Pearson, Alexander T.; Macklin, Paul; Mitchell, Amir; Shmulevich, Ilya; Xie, Lei; Caporaso, J. Gregory (2020-03-01). "The Cancer Microbiome: Distinguishing Direct and Indirect Effects Requires a Systemic View". Trends in Cancer. 6 (3): 192–204. doi: 10.1016/j.trecan.2020.01.004. ISSN  2405-8033. PMC  7098063. PMID  32101723.
  20. ^ Helmink, Beth A.; Khan, M. A. Wadud; Hermann, Amanda; Gopalakrishnan, Vancheswaran; Wargo, Jennifer A. (2019-03-06). "The microbiome, cancer, and cancer therapy". Nature Medicine. 25 (3): 377–388. doi: 10.1038/s41591-019-0377-7. ISSN  1546-170X. PMID  30842679. S2CID  71145949.
  21. ^ Trøseid, Marius; Andersen, Geir Øystein; Broch, Kaspar; Hov, Johannes Roksund (2020-02-01). "The gut microbiome in coronary artery disease and heart failure: Current knowledge and future directions". eBioMedicine. 52: 102649. doi: 10.1016/j.ebiom.2020.102649. ISSN  2352-3964. PMC  7016372. PMID  32062353.
  22. ^ Young, Vincent B. (2017-03-15). "The role of the microbiome in human health and disease: an introduction for clinicians". BMJ. 356: j831. doi: 10.1136/bmj.j831. ISSN  0959-8138. PMID  28298355. S2CID  2443057.
  23. ^ Dheilly, Nolwenn Marie (2014-07-03). "Holobiont–Holobiont Interactions: Redefining Host–Parasite Interactions". PLOS Pathogens. 10 (7): e1004093. doi: 10.1371/journal.ppat.1004093. ISSN  1553-7374. PMC  4081813. PMID  24992663.
  24. ^ Belkaid, Yasmine; Hand, Timothy W. (2014-03-27). "Role of the Microbiota in Immunity and Inflammation". Cell. 157 (1): 121–141. doi: 10.1016/j.cell.2014.03.011. ISSN  0092-8674. PMC  4056765. PMID  24679531.


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