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Nested PCR Detection of Microscopic Life-Stages of Laminarian Macroalgae and Comparison with Adult Forms Along Intertidal Height Gradients

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Nested PCR Detection of Microscopic Life-Stages of Laminarian Macroalgae and Comparison with Adult Forms Along Intertidal Height Gradients MARINE ECOLOGY PROGRESS SERIES Vol. 332: 1–10, 2007 Published March 5 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Nested PCR detection of microscopic life-stages of laminarian macroalgae and comparison with adult forms along intertidal height gradients Caroline H. Fox, Andrew K. Swanson* Department of Biology, Millis Hall, Case Western Reserve University, Cleveland, Ohio 44106, USA ABSTRACT: Recruitment of kelp species (Laminari- ales) to rocky marine habitats relies on the prior establishment of microscopic life-stages (zoospores, gametophytes, gametes and microscopic sporo- phytes). Unlike macroscopic sporophyte stages of kelp, microscopic life-stages have proved difficult to detect and identify in their natural habitat. Using a species-specific PCR-based assay, we developed a method to detect putative microscopic life-stages of 2 northeast Pacific kelp species, Nereocystis luetkeana (Mertens) Postels et Ruprecht and Hedophyllum ses- sile (C. Agardh) Setchell, from rocky intertidal sub- strate samples. Species-specific primers were evalu- ated for specificity and sensitivity. Comparisons of nested and unnested PCR were performed for both species. Nested PCR was used to screen for target species present on rocks obtained along an intertidal height gradient (0.0 to 3.5 m Lowest Low Water Microscopic life-stages of kelp are difficult to identify in [LLW]) from 2 sites at monthly intervals in summer nature. A nested PCR assay was used to detect and monitor 2005. Vertical distribution patterns of the putative the distribution of microscopic life-stages of 2 intertidal microscopic life-stages and the macroscopic sporo- Pacific kelp species, Nereocystis luetkeana and Hedophyllum phyte form were compared at both sites. Putative sessile. This technique is important for assessing zonation pat- microscopic life-stages of N. luetkeana were detected terns, persistence and recovery of kelp species on rocky sub- strates. at both sites and displayed a widespread vertical dis- Photos: Caroline H. Fox & Robert J. J. Davey tribution with no clear spatial or temporal relation- ship. In comparison, H. sessile putative microscopic life-stage distribution was much more spatially INTRODUCTION restricted, showing a similar distribution to the macroscopic sporophyte. This study demonstrates the Members of the order Laminariales, often dominant sensitivity, specificity and validity of utilizing molecu- in rocky nearshore and intertidal zones of temperate lar techniques to describe the distribution of micro- and polar seas, undergo lifecycles that involve the scopic life-stages of certain kelp species. alternation of heteromorphic generations (reviewed in KEY WORDS: Kelp · Nested PCR · Microscopic life- Dayton 1985, Foster & Schiel 1985, Schiel & Foster stages · ITS rDNA · Intertidal 1986, Steneck et al. 2002). Development to the diploid macroscopic sporophyte stage relies on a number Resale or republication not permitted without written consent of the publisher of microscopic life-stages (zoospores, gametophytes, *Corresponding author. Email: [email protected] © Inter-Research 2007 · www.int-res.com 2 Mar Ecol Prog Ser 332: 1–10, 2007 gametes and microscopic sporophytes) and, while A wide array of PCR-based molecular tools have been identification within the Laminariales is largely based used to detect, monitor and map the distribution of upon morphological characters of the macroscopic microorganisms in a range of natural and manipulated sporophyte (Setchell & Gardner 1925), species identifi- environments. Of these tools, nested PCR is a highly cation of microscopic life-stages has proved difficult. sensitive and specific technology, often used to detect Currently, there exists no taxonomy for Laminariales one or more species in environmental samples. For gametophytes (Garbary et al. 1999), embryonic sporo- example, arbuscular mycorrhizal fungi in plant roots phytes or settled zoospores that can be used to identify (van Tuinen et al. 1998), pathenogenic fungi in plant organisms to species, genus or even family levels, tissues (Zhang et al. 2005), seastar larvae in ballast although species discrimination of planktonic kelp zoo- water (Deagle et al. 2003) and a toxic dinoflagellate in spores is possible (Graham 1999, Graham & Mitchell ballast and estuarine samples (Patil et al. 2005) were 1999). Consequently, very little is known about the detected using nested PCR protocols. Using a similar ecology of post-settlement kelp microscopic life-stages, approach, we developed 2 nested PCR protocols for despite their purported influence. the detection of Hedophyllum sessile (C. Agardh) Microscopic life-stages of marine algae may play cru- Setchell and Nereocystis luetkeana (Mertens) Postels cial roles in determining population persistence, distri- et Ruprecht from epilithic and endolithic biofilm com- bution, recovery and dynamics. Referred to as ‘banks munities inhabiting natural intertidal rock substrates. of microscopic forms’ by Chapman (1986), microscopic Using a combination of our nested PCR detection life-stages are thought to function analogously to ter- protocol and intertidal quadrat surveys, we described restrial seedbanks (Edwards 2000), i.e. they are capa- and compared the spatial and temporal distribution of ble of persisting in environmental conditions too macroscopic and putative microscopic life-stages of stressful for the large macrophyte form (Anderson Nereocystis luetkeana and Hedophyllum sessile along 1982, Santelices 1990, Hoffman & Santelices 1991, Kin- a vertical tidal height gradient at 2 locations in Barkley lan et al. 2003). Experimental evidence suggests that Sound, British Columbia, Canada, that differ in wave microscopic life-stages of marine algae may enhance exposure and presence of macroscopic sporophytes. N. recruitment (Edwards 2000), persistence (Edwards luetkeana, considered an annual but often surviving 2000, Kinlan et al. 2003), contribute to recovery follow- longer, is a common subtidal canopy-forming species ing disturbance (Santelices 1990, Santelices et al. 1995, that may grow to over 10 m in length. In contrast, Blanchette 1996, Edwards 2000, Kinlan et al. 2003) and perennial H. sessile sporophytes are small prostrate determine the presence of the macroscopic form (Gra- forms lacking a stipe and are generally found in the ham 1996, Ladah et al. 1999, Edwards 2000, Swanson mid- and low intertidal. Based on the absence of & Druehl 2000). More specifically, studies indicate macroscopic sporophytes at the relatively wave shel- that sensitivities of microscopic life-stages of kelp are tered site, no microscopic life-stages were predicted to related to vertical zonation patterns of the macroscopic occur. In comparison, at the site of higher wave expo- sporophyte form (Swanson & Druehl 2000, Wiencke sure, macroscopic forms of both species persisted, and et al. 2000, 2004, 2006, Roleda et al. 2005), although we predicted that putative microscopic life-stages efforts to characterize natural microscopic life-stage would be present on intertidal rock. However, predict- assemblages along tidal height gradients have been ing the distribution of putative microscopic life-stages hampered by identification constraints. along a tidal height gradient is impeded by a lack of In situ research involving post-settlement micro- prior knowledge regarding specific tolerances of scopic life-stages of Laminariales and closely related microscopic life-stages to environmental parameters, orders generally involves out-planting laboratory cul- necessary sampling intensity to capture the distribu- tured microscopic life-stages (e.g. Hsiao & Druehl tions of the microscopic forms and insight into the time 1973, Reed 1990, Graham 1996, Edwards 2000, required for DNA degradation upon microscopic life- Wiencke et al. 2006), monitoring macroscopic recruit- stage cell death. Nonetheless, given the degree of ment on natural, artificial or manipulated substrates to wave action and turbulence at the exposed site and infer information regarding microscopic life-stages the observation of reproductive (i.e. presence of sori) (e.g. Druehl & Hsiao 1977, Reed et al. 1988, Reed 1990, sporophytes throughout the sampling period, we Graham 1996, Reed et al. 1997, Edwards 2000) and/or predicted that putative microscopic life-stages of both identification of microscopic life-stages to the lowest species would be detected throughout the tidal height taxonomic group possible (e.g. Laminariales; Garbary gradient. To the best of our knowledge, this study et al. 1999). Recently, a conventional PCR-based represents the first attempt to directly detect and approach was used to identify extrageneric epiphytic characterize the distribution of putative microscopic and endophytic kelp gametophytes inhabiting the life-stages of kelp inhabiting natural intertidal sub- thalli of Lessoniopsis littoralis (Lane & Saunders 2005). strates. Fox & Swanson: Microscopic life-stages of laminarians 3 MATERIALS AND METHODS with the exception of the rotary wand, which was rinsed repeatedly with ethanol and sterile water and Two sites (Bluestone Point and Dixon Island) located in then flame dried. Barkley Sound, British Columbia, Canada, were se- Powder from replicate (n = 3) samples was pooled for lected. The maximum predicted tidal flux in this region DNA extraction using the FastDNA® Spin kit for soil is approximately 4.0 m. Both sites have a northwest as- (Q-Biogene) with the optional 15 min extended spin pect and host visibly different macroalgal communities. included and the
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