Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins.
| Title: | Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins. |
|---|---|
| Authors: | Howe-Kerr LI; BioSciences Department, Rice University, Houston, TX, USA. lihowekerr@gmail.com.; Knochel AM; BioSciences Department, Rice University, Houston, TX, USA.; Department of Biological Sciences, Florida International University, Miami, FL, USA.; Meyer MD; Shared Equipment Authority, Rice University, Houston, TX, USA.; Sims JA; BioSciences Department, Rice University, Houston, TX, USA.; Environmental Science and Policy, George Mason University, Fairfax, VA, USA.; Karrick CE; BioSciences Department, Rice University, Houston, TX, USA.; Grupstra CGB; BioSciences Department, Rice University, Houston, TX, USA.; Department of Biology, Boston University, Boston, MA, USA.; Veglia AJ; BioSciences Department, Rice University, Houston, TX, USA.; Department of Biology, University of Puerto Rico, Mayagüez, PR, USA.; Thurber AR; Department of Microbiology, Oregon State University, Corvallis, OR, USA.; College of Earth Ocean and Atmospheric Sciences, Oregon State University, Corvallis, OR, USA.; Vega Thurber RL; Department of Microbiology, Oregon State University, Corvallis, OR, USA.; Correa AMS; BioSciences Department, Rice University, Houston, TX, USA. amsc@berkeley.edu.; Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA. amsc@berkeley.edu. |
| Source: | The ISME journal [ISME J] 2023 Dec; Vol. 17 (12), pp. 2389-2402. Date of Electronic Publication: 2023 Nov 01. |
| Publication Type: | Journal Article; Research Support, Non-U.S. Gov't |
| Language: | English |
| Journal Info: | Publisher: Oxford University Press Country of Publication: England NLM ID: 101301086 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1751-7370 (Electronic) Linking ISSN: 17517362 NLM ISO Abbreviation: ISME J Subsets: MEDLINE |
| Imprint Name(s): | Publication: 2024- : Oxford : Oxford University Press; Original Publication: London : Nature Pub. Group |
| MeSH Terms: | Anthozoa*/genetics ; Dinoflagellida*/genetics; Animals ; Coral Reefs ; Symbiosis ; Oceans and Seas |
| Abstract: | Filamentous viruses are hypothesized to play a role in stony coral tissue loss disease (SCTLD) through infection of the endosymbiotic dinoflagellates (Family Symbiodiniaceae) of corals. To evaluate this hypothesis, it is critical to understand the global distribution of filamentous virus infections across the genetic diversity of Symbiodiniaceae hosts. Using transmission electron microscopy, we demonstrate that filamentous virus-like particles (VLPs) are present in over 60% of Symbiodiniaceae cells (genus Cladocopium) within Pacific corals (Acropora hyacinthus, Porites c.f. lobata); these VLPs are more prevalent in Symbiodiniaceae of in situ colonies experiencing heat stress. Symbiodiniaceae expelled from A. hyacinthus also contain filamentous VLPs, and these cells are more degraded than their in hospite counterparts. Similar to VLPs reported from SCTLD-affected Caribbean reefs, VLPs range from ~150 to 1500 nm in length and 16-37 nm in diameter and appear to constitute various stages in a replication cycle. Finally, we demonstrate that SCTLD-affected corals containing filamentous VLPs are dominated by diverse Symbiodiniaceae lineages from the genera Breviolum, Cladocopium, and Durusdinium. Although this study cannot definitively confirm or refute the role of filamentous VLPs in SCTLD, it demonstrates that filamentous VLPs are not solely observed in SCTLD-affected corals or reef regions, nor are they solely associated with corals dominated by members of a particular Symbiodiniaceae genus. We hypothesize that filamentous viruses are a widespread, common group that infects Symbiodiniaceae. Genomic characterization of these viruses and empirical tests of the impacts of filamentous virus infection on Symbiodiniaceae and coral colonies should be prioritized.; (© 2023. The Author(s).) |
| References: | J Gen Virol. 2017 Mar;98(3):352-354. (PMID: 28366187); Nat Methods. 2016 Jul;13(7):581-3. (PMID: 27214047); Virol J. 2005 Aug 16;2:64. (PMID: 16105179); Front Microbiol. 2020 Sep 30;11:572534. (PMID: 33117317); PLoS One. 2014 Apr 11;9(4):e94297. (PMID: 24728373); Nat Rev Microbiol. 2019 Sep;17(9):569-586. (PMID: 31213707); J Gen Virol. 2020 Apr;101(4):364-365. (PMID: 32134375); ISME Commun. 2023 Apr 3;3(1):27. (PMID: 37009785); Sci Rep. 2023 Apr 10;13(1):5813. (PMID: 37037845); Curr Biol. 2018 May 21;28(10):R619-R634. (PMID: 29787730); Science. 2002 Jun 21;296(5576):2158-62. (PMID: 12077394); J Phycol. 2014 Dec;50(6):984-97. (PMID: 26988781); J Invertebr Pathol. 2017 Jul;147:136-144. (PMID: 27993618); Front Microbiol. 2016 Feb 22;7:127. (PMID: 26941712); Virology. 1997 Sep 29;236(2):296-306. (PMID: 9325237); PeerJ. 2019 May 13;7:e6898. (PMID: 31139503); Nat Commun. 2017 Aug 1;8(1):168. (PMID: 28761042); PeerJ. 2022 Nov 2;10:e14176. (PMID: 36345483); Mol Plant Microbe Interact. 2014 Mar;27(3):215-26. (PMID: 24405034); Environ Microbiol. 2009 Aug;11(8):2148-63. (PMID: 19397678); J Virol. 2008 Oct;82(19):9546-54. (PMID: 18667514); PeerJ. 2023 May 2;11:e15023. (PMID: 37151292); ISME Commun. 2023 Mar 9;3(1):19. (PMID: 36894742); PeerJ. 2023 Aug 23;11:e15836. (PMID: 37637172); PLoS One. 2020 Nov 11;15(11):e0241871. (PMID: 33175886); Microorganisms. 2021 Oct 20;9(11):. (PMID: 34835306); Dis Aquat Organ. 2006 Mar 23;69(1):101-10. (PMID: 16703772); Ecol Evol. 2016 Jan 09;6(2):560-72. (PMID: 26843939); Front Microbiol. 2017 Sep 01;8:1665. (PMID: 28919883); BMC Microbiol. 2017 Aug 17;17(1):174. (PMID: 28818037); Front Microbiol. 2020 Apr 23;11:681. (PMID: 32425901); Sci Rep. 2016 Aug 10;6:31374. (PMID: 27506875); ISME J. 2013 Jan;7(1):13-27. (PMID: 22791238); PeerJ. 2018 May 23;6:e4816. (PMID: 29844969); Front Microbiol. 2019 Sep 24;10:2244. (PMID: 31608047); Nat Rev Microbiol. 2017 Apr;15(4):205-216. (PMID: 28090075); Proc Natl Acad Sci U S A. 2021 Feb 2;118(5):. (PMID: 33500354); J Microbiol. 2008 Jun;46(3):235-43. (PMID: 18604491); Glob Chang Biol. 2022 Feb;28(4):1342-1358. (PMID: 34908214); Dis Aquat Organ. 2014 Dec 2;112(2):149-59. (PMID: 25449326); ISME Commun. 2022 May 30;2(1):46. (PMID: 37938315); Sci Rep. 2022 Nov 10;12(1):19248. (PMID: 36357458); Commun Biol. 2022 Jun 9;5(1):440. (PMID: 35681037); Environ Microbiol. 2022 Mar;24(3):1166-1182. (PMID: 34431191); Environ Microbiol. 2015 Oct;17(10):3440-9. (PMID: 25708646); Front Microbiol. 2020 Oct 26;11:569354. (PMID: 33193161); Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18413-8. (PMID: 19017800); Front Microbiol. 2020 May 26;11:847. (PMID: 32528423); Nat Commun. 2023 May 22;14(1):2915. (PMID: 37217477); Mol Ecol Resour. 2019 Jul;19(4):1063-1080. (PMID: 30740899); ISME J. 2022 May;16(5):1430-1441. (PMID: 35046559); Appl Environ Microbiol. 2007 May;73(9):2976-81. (PMID: 17351090); Microbiol Resour Announc. 2022 Feb 17;11(2):e0119921. (PMID: 35175123); Annu Rev Phytopathol. 2007;45:73-100. (PMID: 17362202); Nat Commun. 2020 Sep 15;11(1):4626. (PMID: 32934228) |
| Grant Information: | 1635913 National Science Foundation (NSF); 1933165 National Science Foundation (NSF); 1635798 National Science Foundation (NSF); 2145472 National Science Foundation (NSF) |
| Molecular Sequence: | SRA PRJNA955224 |
| Entry Date(s): | Date Created: 20231101 Date Completed: 20231204 Latest Revision: 20250923 |
| Update Code: | 20260130 |
| PubMed Central ID: | PMC10689786 |
| DOI: | 10.1038/s41396-023-01526-6 |
| PMID: | 37907732 |
| Database: | MEDLINE |
Journal Article; Research Support, Non-U.S. Gov't