The gut microbiome of freshwater Unionidae mussels is determined by host species and is selectively retained from filtered seston


Autoři: Eric A. Weingarten aff001;  Carla L. Atkinson aff002;  Colin R. Jackson aff001
Působiště autorů: Department of Biology, University of Mississippi, University, Mississippi, United States of America aff001;  Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224796

Souhrn

Freshwater mussels are a species-rich group of aquatic invertebrates that are among the most endangered groups of fauna worldwide. As filter-feeders that are constantly exposed to new microbial inoculants, mussels represent an ideal system to investigate the effects of species or the environment on gut microbiome composition. In this study, we examined if host species or site exerts a greater influence on microbiome composition. Individuals of four co-occurring freshwater mussel species, Cyclonaias asperata, Fusconaia cerina, Lampsilis ornata, and Obovaria unicolor were collected from six sites along a 50 km stretch of the Sipsey River in Alabama, USA. High throughput 16S rRNA gene sequencing revealed that mussel gut bacterial microbiota were distinct from bacteria on seston suspended in the water column, and that the composition of the gut microbiota was influenced by both host species and site. Despite species and environmental variation, the most frequently detected sequences within the mussel microbiota were identified as members of the Clostridiales. Sequences identified as the nitrogen-fixing taxon Methylocystis sp. were also abundant in all mussel species, and sequences of both bacterial taxa were more abundant in mussels than in water. Site physicochemical conditions explained almost 45% of variation in seston bacterial communities but less than 8% of variation in the mussel bacterial microbiome. Together, these findings suggest selective retention of bacterial taxa by the freshwater mussel host, and that both species and the environment are important in determining mussel gut microbiome composition.

Klíčová slova:

Bacteria – Bivalves – Clostridium – Fresh water – Gut bacteria – Microbiome – Mussels – Species diversity


Zdroje

1. Williams JD, Bogan AE, Garner JT. Freshwater mussels of Alabama and the Mobile basin in Georgia, Mississippi, and Tennessee. Tuscaloosa: University of Alabama Press; 2008

2. Neves RJ, Bogan AE, Williams JD, Ahlstedt SA, Hartfield PW. Status of aquatic mollusks in the southeastern United States: a downward spiral of diversity. In: Benz GW, Collins DE, editors. Aquatic fauna in peril: the southeastern perspective. Decatur: Southeast Aquatic Research Institute, Lenz Design and Communications; 1997. pp. 44–86.

3. Parmalee PW, Bogan AE. Freshwater mussels of Tennessee. Knoxville: University of Tennessee Press; 1998.

4. Strayer DL, Downing JA, Haag WR, King TL, Layzer JB, Newton TJ, et al. Changing perspectives on pearly mussels, North America's most imperiled animals. Biosci. 2004;54: 429–439.

5. Dudgeon D, Arthington AH, Gessner MO, Kawabata Z, Knowler DJ, Lévêque C, et al. Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev. 2006;81: 163–182. doi: 10.1017/S1464793105006950 16336747

6. Atkinson CL, Julian JP, Vaughn CC. Species and function lost: Role of drought in structuring stream communities. Biol Conserv. 2014;176: 30–38.

7. Vaughn CC, Hakenkamp CC. The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol. 2001;46: 1431–1446.

8. Atkinson CL, Sansom BJ, Vaughn CC, Forshay KJ. Consumer aggregations drive nutrient dynamics and ecosystem metabolism in nutrient-limited systems. Ecosystems. 2018;21: 521–535.

9. Atkinson CL, Vaughn CC, Forshay KJ, Cooper JT. Aggregated filter‐feeding consumers alter nutrient limitation: consequences for ecosystem and community dynamics. Ecology. 2013;94: 1359–1369. doi: 10.1890/12-1531.1 23923499

10. Atkinson CL, Vaughn CC. Biogeochemical hotspots: temporal and spatial scaling of the impact of freshwater mussels on ecosystem function. Freshw Biol. 2015;60: 563–574.

11. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangle JL, et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA. 2013;110: 6548–6553. doi: 10.1073/pnas.1302837110 23576752

12. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA. 2015;112; E911–E920. doi: 10.1073/pnas.1414592112 25605935

13. Rietl AJ, Overlander ME, Nyman AJ, Jackson CR. Microbial community composition and extracellular enzyme activities associated with Juncus roemerianus and Spartina alterniflora vegetated sediments in Louisiana saltmarshes. Microb Ecol. 2016;71: 290–303. doi: 10.1007/s00248-015-0651-2 26271740

14. King GM, Judd C, Kuske CR, Smith C. Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA. PLoS One. 2012;7: 1–11. doi: 10.1371/journal.pone.0051475 23251548

15. Pierce ML, Ward JE, Holohan BA, Zhao X, Hicks RE. The influence of site and season on the gut and pallial fluid microbial communities of the eastern oyster, Crassostrea virginica (Bivalvia, Ostreidae): community-level physiological profiling and genetic structure. Hydrobiologia. 2016;765: 97–113.

16. Ossai S, Ramachandran P, Ottesen A, Reed E, DePaola A, Parveen S. Microbiomes of American Oysters (Crassostrea virginica) harvested from two sites in the Chesapeake Bay. Genome Announc. 2017;5: e00729–17. doi: 10.1128/genomeA.00729-17 28751404

17. Chauhan A, Wafula D, Lewis DE, Pathak A. Metagenomic assessment of the Eastern oyster-associated microbiota. Genome Announc. 2014;2: e01083–14. doi: 10.1128/genomeA.01083-14 25342691

18. Thomas JC, Wafula D, Chauhan A, Green SJ, Gragg R, Jagoe C. A survey of deepwater horizon (DWH) oil-degrading bacteria from the Eastern oyster biome and its surrounding environment. Front Microbiol. 2014;5: 149. doi: 10.3389/fmicb.2014.00149 24782841

19. Wegner KM, Volkenborn N, Peter H, Eiler A. Disturbance induced decoupling between host genetics and composition of the associated microbiome. BMC Microbiol. 2013;13: 252. doi: 10.1186/1471-2180-13-252 24206899

20. Lokmer A, Goedknegt MA, Thieltges DW, Fiorentino D, Kuenzel S, Baines JF, et al. Spatial and temporal dynamics of Pacific oyster hemolymph microbiota across multiple scales. Front Microbiol. 2016;7: 1367. doi: 10.3389/fmicb.2016.01367 27630625

21. Trabal Fernández N, Mazón-Suástegui JM, Vázquez-Juárez R, Ascencio-Valle F, Romero J. Changes in the composition and diversity of the bacterial microbiota associated with oysters (Crassostrea corteziensis, Crassostrea gigas and Crassostrea sikamea) during commercial production. FEMS Microbiol Ecol. 2014;88: 69–83. doi: 10.1111/1574-6941.12270 24325323

22. Lokmer A, Wegner KM. Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. ISME J. 2015;9: 670–682. doi: 10.1038/ismej.2014.160 25180968

23. King WL, Siboni N, Williams NLR, Kahlke T, Nguyen KV, Jenkins C, et al. Variability in the composition of Pacific Oyster microbiomes across oyster families exhibiting different levels of susceptibility to OsHV-1 μvar disease. Front Microbiol. 2019;10: 473. doi: 10.3389/fmicb.2019.00473 30915058

24. Vaughn CC, Nichols SJ, Spooner DE. Community and foodweb ecology of freshwater mussels. J North Am Benthol Soc. 2008;27: 409–423.

25. Murphy AE, Kolkmeyer R, Song B, Anderson IC, Bowen J. Bioreactivity and Microbiome of Biodeposits from Filter-Feeding Bivalves. Microb Ecol. 2019;77: 343–357. doi: 10.1007/s00248-018-01312-4 30612185

26. McCullagh WH, Williams JD, McGregor SW, Pierson JM, Lydeard C. The Unionid (Bivalvia) fauna of the Sipsey River in northwestern Alabama, an aquatic hotspot. Am Malacol Bull. 2002;17: 1–15.

27. Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP, McDermott TR. Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ Microbiol 2001;3: 532–542. doi: 10.1046/j.1462-2920.2001.00221.x 11578314

28. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79: 5112–5120. doi: 10.1128/AEM.01043-13 23793624

29. Stone BWG, Jackson CR. Biogeographic patterns between bacterial phyllosphere communities of the Southern Magnolia (Magnolia grandiflora) in a small forest. Microb Ecol. 2016;71: 954–961. doi: 10.1007/s00248-016-0738-4 26883131

30. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75: 7537–7541. doi: 10.1128/AEM.01541-09 19801464

31. Schloss PD, Gevers D, Westcott SL. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One. 2011;6: 1–14. doi: doi.org/10.1371/journal.pone.0027310

32. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41: D590–D596. doi: 10.1093/nar/gks1219 23193283

33. Maidak BL, Cole JR, Lilburn TG, Parker CT Jr, Saxman PR, Stredwick JM, et al. The RDP (ribosomal database project) continues. Nucleic Acids Res. 2000;28, 173–174. doi: 10.1093/nar/28.1.173 10592216

34. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P. et al. The vegan package, community ecology package 2008;10: 631–637.

35. Team RC. R: A language and environment for statistical computing. 2013

36. Cao R, Xue CH, Liu Q, Xue Y. Microbiological, chemical, and sensory assessment of Pacific Oysters (Crassostrea gigas) stored at different temperatures. Czech J Food Sci. 2009;27: 102–108.

37. Olafsen JA, Mikkelsen HV, Giæver HM, Hansen GH. Indigenous bacteria in hemolymph and tissues of marine bivalves at low temperatures. Appl Environ Microbiol. 1993;59: 1848–1854. 16348962

38. Aceves AK, Johnson P, Bullard SA, Lafrentz S, Arias CR. Description and characterization of the digestive gland microbiome in the freshwater mussel Villosa nebulosa (Bivalvia: Unionidae). J Molluscan Stud. 2019;84: 240–246.

39. Miller WA, Miller MA, Gardner IA, Atwill ER, Byrne BA, Jang S, et al. Salmonella spp., Vibrio spp., Clostridium perfringens, and Plesiomonas shigelloides in Marine and Freshwater Invertebrates from Coastal California Ecosystems. Microb Ecol. 2006;52: 198–206. doi: 10.1007/s00248-006-9080-6 16897302

40. Green TJ, Siboni N, King WL, Labbate M, Seymour JR, Raftos D. Simulated marine heat wave alters abundance and structure of Vibrio populations associated with the Pacific Oyster resulting in a mass mortality event. Microb Ecol. 2019;77: 736–747. doi: 10.1007/s00248-018-1242-9 30097682

41. King WL, Jenkins C, Go J, Siboni N, Seymour JR, Labbate M. Characterisation of the Pacific Oyster microbiome during a summer mortality event. Microb Ecol. 2019;77: 502–512. doi: 10.1007/s00248-018-1226-9 29987529

42. Colston RJ, Jackson CR. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol. 2016;25: 3776–3800. doi: 10.1111/mec.13730 27297628

43. König S, Gros O, Heiden SE, Hinzke T, Thürmer A, Poehlein A, et al. Nitrogen fixation in a chemoautotrophic lucinid symbiosis. Nat Microbiol. 2016;2: 16193. doi: 10.1038/nmicrobiol.2016.193 27775698

44. Moulton OM, Altabet MA, Beman JM, Deegan LA, Lloret J, Lyons MK. et al. Microbial associations with macrobiota in coastal ecosystems: patterns and implications for nitrogen cycling. Front Ecol Environ. 2016;14: 200–208.

45. Belova SE, Kulichevskaya IS, Bodelier PL, and Dedysh SN. Methylocystis bryophila sp. nov., a facultatively methanotrophic bacterium from acidic Sphagnum peat, and emended description of the genus Methylocystis (ex Whittenbury et al. 1970) Bowman et al. 1993. International journal of systematic and evolutionary microbiology, 2013;63, 1096–1104. doi: 10.1099/ijs.0.043505-0 22707532

46. Dam B, Dam S, Blom J, and Liesack W. Genome analysis coupled with physiological studies reveals a diverse nitrogen metabolism in Methylocystis sp. strain SC2. PLoS One. 2013;8, e74767. doi: 10.1371/journal.pone.0074767 24130670

47. Black EM, Chimenti MS, Just CL. Effect of freshwater mussels on the vertical distribution of anaerobic ammonia oxidizers and other nitrogen-transforming microorganisms in upper Mississippi river sediment. PeerJ 2017;5: e3536. doi: 10.7717/peerj.3536 28717594

48. Augspurger T, Keller AE, Black MC, Cope WG, Dwyer FJ. Water quality guidance for protection of freshwater mussels (Unionidae) from ammonia exposure. Environ Toxicol Chem. 2003;22: 2569–2575. doi: 10.1897/02-339 14587894

49. Allen DC, Vaughn CC. Burrowing behavior of freshwater mussels in experimentally manipulated communities. J North Am Benthol Soc. 2009;28: 93–100.

50. Pfeiffer JM, Atkinson CL, Sharpe AE, Capps KA, Emery KF, Page LM. Phylogeny of Mesoamerican freshwater mussels and a revised tribe‐level classification of the Ambleminae. Zool Scr. 2019;48: 106–117.

51. Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, Stombaugh J, et al. Moving pictures of the human microbiome. Genome Biol. 2011;12: R50. doi: 10.1186/gb-2011-12-5-r50 21624126


Článek vyšel v časopise

PLOS One


2019 Číslo 11