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Life Without a Cell Membrane: Challenging the Specificity of Bacterial Endophytes Within Bryopsis (Bryopsidales, Chlorophyta)

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Life Without a Cell Membrane: Challenging the Specificity of Bacterial Endophytes Within Bryopsis (Bryopsidales, Chlorophyta) See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/51818564 Life without a cell membrane: Challenging the specificity of bacterial endophytes within Bryopsis (Bryopsidales, Chlorophyta) Article in BMC Microbiology · November 2011 DOI: 10.1186/1471-2180-11-255 · Source: PubMed CITATIONS READS 23 85 5 authors, including: Joke Hollants Helen Decleyre MindBytes 9 PUBLICATIONS 89 CITATIONS 16 PUBLICATIONS 244 CITATIONS SEE PROFILE SEE PROFILE Frederik Leliaert Olivier De Clerck Meise Botanic Garden Ghent University 242 PUBLICATIONS 4,218 CITATIONS 273 PUBLICATIONS 5,022 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: MICROBIAN View project Bioplastic production by thermophiles, IMMB, University of Munster, Munster, germany View project All content following this page was uploaded by Helen Decleyre on 02 June 2014. The user has requested enhancement of the downloaded file. Hollants et al. BMC Microbiology 2011, 11:255 http://www.biomedcentral.com/1471-2180/11/255 RESEARCHARTICLE Open Access Life without a cell membrane: Challenging the specificity of bacterial endophytes within Bryopsis (Bryopsidales, Chlorophyta) Joke Hollants1,2*, Helen Decleyre1, Frederik Leliaert2, Olivier De Clerck2 and Anne Willems1 Abstract Background: The siphonous green macroalga Bryopsis has some remarkable characteristics. Besides hosting a rich endophytic bacterial flora, Bryopsis also displays extraordinary wound repair and propagation mechanisms. This latter feature includes the formation of protoplasts which can survive in the absence of a cell membrane for several minutes before regenerating into new individuals. This transient ‘life without a membrane’ state, however, challenges the specificity of the endophytic bacterial communities present and raises the question whether these bacteria are generalists, which are repeatedly acquired from the environment, or if there is some specificity towards the Bryopsis host. Results: To answer this question, we examined the temporal stability and the uniqueness of endobiotic bacterial communities within Bryopsis samples from the Mexican west coast after prolonged cultivation. DGGE analysis revealed that Bryopsis endophytic bacterial communities are rather stable and clearly distinct from the epiphytic and surrounding cultivation water bacterial communities. Although these endogenous communities consist of both facultative and obligate bacteria, results suggest that Bryopsis owns some intrinsic mechanisms to selectively maintain and/or attract specific bacteria after repeated wounding events in culture. Conclusions: This suggests that Bryopsis algae seem to master transient stages of life without a cell membrane well as they harbor specific - and possibly ecological significant - endophytic bacteria. Background Arcobacter, Bacteroidetes, Flavobacteriaceae, Myco- The marine green alga Bryopsis has long been suspected plasma, Labrenzia, Phyllobacteriaceae and Xanthomona- to harbor endogenous bacteria. These intracellular bac- daceae species. Moreover, the same Bacteroidetes, teria have been repeatedly observed in the cytoplasm as Mycoplasma, Phyllobacteriaceae, and in particular Flavo- well as vacuolar regions of algal thalli and gametes by bacteriaceae bacteria, were detected in several Bryopsis electron microscopy [[1,2] and personal observations see samples collected hundreds of kilometers apart. This additional file 1], suggesting the presence of bacterial apparent spatial stability of the Bryopsis-bacterial endo- endophytes within Bryopsis is a natural phenomenon. biosis, however, raises the question whether these endo- Recently, the first insights were provided into the iden- phytes are a subset of the free-living bacterial tity and diversity of these bacterial endophytes within community or whether there is some specificity towards two Bryopsis species from the Pacific Mexican coast [3]. the Bryopsis host. Although the distinctiveness between Full length 16S rRNA gene analysis showed that the free-living and macroalgal-associated bacterial commu- Bryopsis endophytic bacterial communities are quite low nities is well established [4-8], the extraordinary mor- in diversity (i.e. only 7 bacterial OTUs detected) but tax- phological and physiological characteristics of the onomically wide-ranging with the presence of Bryopsis host must have implications for the specificity of its bacterial endophytes. Bryopsis is a marine sipho- * Correspondence: [email protected] nous macroalga composed of a single, tubular shaped 1Laboratory of Microbiology, Department of Biochemistry and Microbiology, cell which contains multiple nuclei and chloroplasts in a Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium thin cytoplasmic layer surrounding a large central Full list of author information is available at the end of the article © 2011 Hollants et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Hollants et al. BMC Microbiology 2011, 11:255 Page 2 of 10 http://www.biomedcentral.com/1471-2180/11/255 vacuole [9]. While an organism composed of a giant, culture that had been cultivated for two years (i.e. in single cell would be prone to damage, siphonous macro- February 2011). These cultivation water samples were algae possess an intricate defense network that operates serially filtered over a syringe filter holder with sterile at various levels [7,10]. In Bryopsis, for example, the 11 μm and 0.2 μm cellulose acetate filters (Sartorius Ste- metabolite kahalalide F, which shows in vitro therapeu- dim Biotech GmbH, Germany) to remove small Bryopsis tic activities, protects the alga from fish predation [11]. fragments and to retain the planktonic microbial frac- Even if damage does occur, a complex, multistep wound tion, respectively. Bacterial DNA was extracted from the response is triggered [10,12] to which Bryopsis algae add 0.2 μm filters using the bead-beating method followed a surprisingly feature, i.e. the formation of protoplasts by phenol extraction and ethanol precipitation as [13]. These protoplasts are membraneless structures that described by Zwart et al. [17]. Parallel with these culti- can survive in seawater for 10-20 minutes. Subsequently, vation water samples, washing water samples were membranes and a cell wall are synthesized de novo sur- obtained from all five MX isolates by repeatedly vortex- rounding each protoplast, which then develop into new ing the algae in 50 ml sterile artificial seawater (ASW). Bryopsis plants. This not only suggests Bryopsis can These washing water samples, containing the loosely exist - at least transiently -without a cell membrane, it Bryopsis-associated bacterial fraction, were processed as also questions the nature of the association between the described above. Subsequently, approximately 1 gram of algal host and the endophytic bacterial communities each washed Bryopsis MX sample was placed in 500 μl present. Are these bacteria Bryopsis-specific, obligate cetyltrimethylammonium bromide (CTAB) lysis buffer endophytes (specialists) or are they rather generalists supplemented with 20 mg.mL-1 proteinase K and 2.5 μl (facultative endogenous bacteria) which are repeatedly filter-sterilized Umonium Master (Huckert’sInterna- acquired from the local environment (epiphytic commu- tional, Belgium) to eliminate the epiphytic bacterial frac- nities and/or surrounding sea water)? tion from the Bryopsis surface [15]. Samples were To address this issue, we evaluated the temporal stabi- incubated for 30 minutes at 60°C and subsequently vor- lity of the endobiotic bacterial communities after pro- texed in 500 μl sterile ASW for 2 minutes. Algal mate- longed cultivation of Bryopsis isolates. We also rial was removed by centrifugation and the examined the diversity of the epiphytic and surrounding supernatants’ DNA originated from the epiphytic bacter- water bacterial communities of five Bryopsis isolates in ial fraction was extracted using a CTAB protocol modi- culture using the DGGE technique and subsequently fied from Doyle and Doyle [16]. compared these DGGE profiles with previously obtained DGGE banding patterns of Bryopsis endophytic bacterial DGGE and sequence analysis communities [3]. Theendophytic(EN-2010),epiphytic(EP),washing water (WW) and cultivation water (CW) bacterial com- Methods munity extracts were subjected to a nested-PCR DGGE Sample collection and DNA extraction approach. First, full length 16S rRNA gene amplification Bryopsis hypnoides (MX19 and MX263) and Bryopsis was carried out with the universal bacterial primers pennata var. leprieurii individuals (MX90, MX164 and 27F/1492R following the protocol outlined in Lane [18]. MX344) were collected in February 2009 at five different PCR amplicons were purified using a Nucleofast 96 PCR sites along the Mexican west coast [3]. Living algal sam- clean up membrane system (Machery-Nagel, Germany) ples were transferred to the laboratory and unialgal according to the manufacturer’s instructions and subse- Bryopsis cultures were formed by repeatedly isolating quently submitted to a second PCR with primer pair clean apical fragments. To preserve these unialgal cul- F357-GC/R518 targeting the V3 region of the 16S rRNA tures, apical fragments
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