Core and Dynamic Microbial Communities of Two Invasive Ascidians: Can Host–Symbiont Dynamics Plasticity Affect Invasion Capacity?
Ascidians (Chordata, Ascidiacea) are considered to be prominent marine invaders, able to tolerate highly polluted environments and fluctuations in salinity and temperature. Here, we examined the seasonal and spatial dynamics of the microbial communities in the inner-tunic of two invasive ascidians, Styela plicata (Lesueur 1823) and Herdmania momus (Savigny 1816), in order to investigate the changes that occur in the microbiome of non-indigenous ascidians in different environments. Microbial communities were characterized using next-generation sequencing of partial (V4) 16S rRNA gene sequences. A clear differentiation between the ascidian-associated microbiome and bacterioplankton was observed, and two distinct sets of operational taxonomic units (OTUs), one core and the other dynamic, were recovered from both species. The relative abundance of the dynamic OTUs in H. momus was higher than in S. plicata, for which core OTU structure was maintained independently of location. Ten and seventeen core OTUs were identified in S. plicata and H. momus, respectively, including taxa with reported capabilities of carbon fixing, ammonia oxidization, denitrification, and heavy-metal processing. The ascidian-sourced dynamic OTUs clustered in response to site and season but significantly differed from the bacterioplankton community structure. These findings suggest that the associations between invasive ascidians and their symbionts may enhance host functionality while maintaining host adaptability to changing environmental conditions.
KeywordsIntroduced species Microbiome Tunicate Lessepsian invasion Herdmania momus Styela plicata
We thank L. Reshef, P. Erwin, and E. Sieradzki for their comments and advice. We thank S. Meiri and G. Vered for technical assistance and N. Paz for editorial assistance.
H.D., N.S. and S.L.L. designed this study. H.D., L.N., and J.S.E. collected samples. J.S.E. assisted in sequence processing. H.D. conducted the analyses and led the writing of the manuscript. All authors contributed critically to all drafts and gave final approval for publication.
Funding for this project was provided by the US-Israel Binational Science Foundation (BSF), Jerusalem, Israel (number 2014025), to S.L.L. and N.S.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- 12.Wilkinson CR (1978) Microbial associations in sponges. II. Numerical analysis of sponge and water bacterial populations. Mar Biol 49:169–176. https://doi.org/10.1007/BF00387116
- 15.Prieur D, Mével G, Nicolas JL et al (1990) Interactions between bivalve molluscs and bacteria in the marine environment. Oceanogr. Mar. Biol. Annu. Rev. 28:277–352Google Scholar
- 18.Schmidt EW, Obraztsova AY, Davidson SK, Faulkner DJ, Haygood MG (2000) Identification of the antifungal peptide-containing symbiont of the marine sponge Theonella swinhoei as a novel δ-proteobacterium, “Candidatus Entotheonella palauensis.”. Mar. Biol. 136:969–977. https://doi.org/10.1007/s002270000273 Google Scholar
- 27.Galbreath JGMS, Smith JE, Terry RS et al (2004) Invasion success of Fibrillanosema crangonycis, n.sp., n.g.: a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. Int. J. Parasitol. 34:235–244. https://doi.org/10.1016/j.ijpara.2003.10.009 Google Scholar
- 30.Erwin PM, Pineda MC, Webster N, et al (2013) Small core communities and high variability in bacteria associated with the introduced ascidian Styela plicata. Symbiosis 59:35–46. https://doi.org/10.1007/s13199-012-0204-0
- 31.Vrijenhoek RC (2010) Genetics and evolution of deep-sea chemosynthetic bacteria and their invertebrate hosts. The vent and seep biota, topics in geobiology. Springer, Dordrecht, pp 15–49Google Scholar
- 33.Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O'Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu. Rev. Ecol. Syst. 32:305–332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037 Google Scholar
- 34.Lambert G (2001) A global overview of ascidian introductions and their possible impact on the endemic fauna. The biology of ascidians. Springer Japan, Tokyo, pp 249–257Google Scholar
- 35.Monniot C, Monniot F, Laboute P (1991) Coral reef ascidians of New Caledonia. Orstom, ParisGoogle Scholar
- 40.Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Bio Ecol 342:3–4Google Scholar
- 47.Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the southern California Bight. Mar. Ecol. Prog. Ser. 259:145–161Google Scholar
- 48.Schmidt EW, Nelson JT, Rasko DA, Sudek S, Eisen JA, Haygood MG, Ravel J (2005) Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc. Natl. Acad. Sci. U. S. A. 102:7315–7320. https://doi.org/10.1073/pnas.0501424102 Google Scholar
- 52.Hirose E, Maruyama T (2004) What are the benefits in the ascidian-Prochloron symbiosis? Endocytobiosis Cell Res 15:51–62Google Scholar
- 55.Pérès J (1958) Ascidies recoltées sur les côtes Méditerranéennes d’Israel. Bull Res Counc Isr B 7:143–150Google Scholar
- 56.Por FD (1978) Lessepsian migration. The influx of Red Sea biota into the Mediterranean by way of the Suez Canal. Springer-Verlag, BerlinGoogle Scholar
- 60.Gewing M-T, Rothman SBS, Nagar LR et al (2014) Early stages of establishment of the non-indigenous ascidian Herdmania momus (Savigny, 1816) in shallow and deep water environments on natural substrates in the Mediterranean Sea. BioInv Rec 3:77–81. https://doi.org/10.3391/bir.2014.3.2.04 Google Scholar
- 63.Novak L, López-Legentil S, Sieradzki E, Shenkar N (2017) Rapid establishment of the non-indigenous ascidian Styela plicata and its associated bacteria in marinas and fishing harbors along the Mediterranean coast of Israel. Mediterr. Mar. Sci. 18:324–331. https://doi.org/10.12681/mms.2135 Google Scholar
- 64.Dror H (2017) Hidden allies : the potential contribution of bacterial communities to the successful establishment of the invasive ascidians Styela plicata and Herdmania momus in the Eastern Mediterranean. (MSc thesis). Tel-Aviv University, Tel-Aviv, IsraelGoogle Scholar
- 67.Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq illumina sequencing platform. Appl. Environ. Microbiol. 79:5112–5120. https://doi.org/10.1128/AEM.01043-13 Google Scholar
- 72.Oksanen J, Blanchet FG, Kindt R, et al (2016) Package “vegan”: community ecology packageGoogle Scholar
- 82.Kühl M, Behrendt L, Trampe E, Qvortrup K, Schreiber U, Borisov SM, Klimant I, Larkum AWD (2012) Microenvironmental ecology of the chlorophyll b-containing symbiotic cyanobacterium Prochloron in the didemnid ascidian Lissoclinum patella. Front. Microbiol. 3:402. https://doi.org/10.3389/fmicb.2012.00402 Google Scholar
- 94.Neave MJ, Streten-Joyce C, Glasby CJ, McGuinness KA, Parry DL, Gibb KS (2012) The bacterial community associated with the marine polychaete Ophelina sp.1 (Annelida: Opheliidae) is altered by copper and zinc contamination in sediments. Microb. Ecol. 63:639–650. https://doi.org/10.1007/s00248-011-9966-9 Google Scholar
- 96.Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, Webster N, Hentschel U, Taylor MW (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576. https://doi.org/10.1038/ismej.2011.116 Google Scholar
- 97.Pujalte MJ, Lucena T, Ruvira MA, Arahal DR, Macián MC (2014) The family Rhodobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt ETF (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Berlin, pp 439–512Google Scholar
- 101.Kelly LW, Williams GJ, Barott KL, Carlson CA, Dinsdale EA, Edwards RA, Haas AF, Haynes M, Lim YW, McDole T, Nelson CE, Sala E, Sandin SA, Smith JE, Vermeij MJA, Youle M, Rohwer F (2014) Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc. Natl. Acad. Sci. 111:10227–10232. https://doi.org/10.1073/pnas.1403319111 Google Scholar