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Gas Composition of Developing Pneumatocysts in Bull Kelp Nereocystis Luetkeana (Phaeophyceae)1

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Gas Composition of Developing Pneumatocysts in Bull Kelp Nereocystis Luetkeana (Phaeophyceae)1 J. Phycol. 56, 1367–1372 (2020) © 2020 Phycological Society of America DOI: 10.1111/jpy.13037-19-219 NOTE GAS COMPOSITION OF DEVELOPING PNEUMATOCYSTS IN BULL KELP NEREOCYSTIS LUETKEANA (PHAEOPHYCEAE)1 Lauran M. Liggan ,2 and Patrick T. Martone Department of Botany and Biodiversity Research Centre, University of British Columbia, 3529-6270 University Blvd, Vancouver, BC V6T 1Z4, Canada The subtidal kelp Nereocystis luetkeana (hereafter The bull kelp Nereocystis luetkeana (hereafter Nereo- Nereocystis) maintains an upright stature by producing a cystis) builds unique subtidal forests in the Northeast single gas-filled float (pneumatocyst) that provides Pacific by having a singular gas-filled float called a buoyancy. The ability of Nereocystis pneumatocysts to pneumatocyst, which enables the kelp’s flexible thal- inflate with gas underwater is peculiar, and the gas lus to remain upright and vertical in the water col- composition of pneumatocysts has been the topic of umn (Arzee et al. 1985). The ability of this seaweed several studies over the last 100 years. Past studies of to create an air-tight reservoir and inflate underwa- pneumatocyst gases only examined large sporophytes, ter is remarkable, and the gas composition of Nereo- leaving open questions about the origins of these gases cystis pneumatocysts has been the topic of several and how gas composition may change during studies during the first half of the 20th century (Frye development. In this study, we use developmental time et al. 1915, Langdon 1917, Langdon and Gailey as a means to understand the origin and physiological 1920, Rigg and Henry 1935, Rigg and Swain 1941). mechanisms that give rise to different gases within Past studies found that 20–25% of gas sampled from ~ Nereocystis pneumatocysts. Total gas composition was pneumatocysts was oxygen (O2) and 70% or more measured across a range of pneumatocyst sizes (5– was nitrogen (N2), with both gases present in con- 725 mL). Contrary to previous studies that centrations similar to air (Rigg and Henry 1935, Rigg documented pneumatocyst gas concentrations to be and Swain 1941). In addition, up to 13% of the gas similar to air, this study found internal gas levels of CO, was CO, thought to be a product of cell degradation Æ Æ CO2,andO2 to be 1.2 0.8%, 0.6 0.2%, and (autolysis) from the rapidly expanding pneumatocyst 59.9 Æ 13.6%, respectively. Our data suggest that the during early development (Foreman 1976), and 2– composition of gases does not change as 7% of the gas was carbon dioxide (CO2), shown to pneumatocysts grow and that the rate of each gas be a product of cellular respiration (Langdon and added is approximately proportional to changes in Gailey 1920, Rigg and Swain 1941). pneumatocyst volume. Therefore, cells constituting the Gas-filled structures are commonly found in Lami- pneumatocyst wall are likely producing more gas (per nariales and Fucales, where the structure provides surface area) to fill pneumatocysts as they expand, mechanical support to flexible thalli, allowing maintaining proportional gas composition and blades to efficiently access sunlight near the waters’ corresponding internal pressure. surface (Dromgoole 1981a, Stevens et al. 2002, Ste- Key index words: wart 2006, Burnett and Koehl 2017). Most macroal- buoyancy; carbon dioxide; carbon gal pneumatocysts develop from meristematic blade monoxide; development; gas bladder; macroalgae; tissue, forming an organ that generally subtends the oxygen; photosynthesis; physiology; respiration blades (Dromgoole 1981a). However, some genera Abbreviations C C : 1, measured gas concentration; 2, such as Durvillaea, Turbinaria, and Eualaria modify C unknown pneumatocyst gas concentration; gas, gas their blades, by having tissue that separates to form concentration; ggas, grams of gas; kPa, kilopascals; hollow spaces with in the blade itself (Smith 2002, M P gas, molar mass of gas; gas, gas partial pressure; Stevens et al. 2002, Stewart 2004, Stewart et al. V V R, gas constant; 1, volume of the flask; 2, volume 2007). Though pneumatocyst morphology and posi- V of gas sample; p, pneumatocyst volume; ggas, mols tion varies greatly between species and groups, the of gas same buoyant function is achieved. Nereocystis thalli, like most other kelps, initially develop a simple holdfast, stipe, and blade. Pneumatocysts begin to form at the transition zone between the stipe and the blade when sporophytes are no less than 15 cm, 1Received 10 October 2019. Accepted 17 May 2020. Published Online 22 May 2020, Wiley Online Library (wileyonlinelibrary.com). in length, about 2 weeks after germination (Nichol- 2Author for correspondence: e-mail [email protected]. son 1970, Dromgoole 1981a, Liggan and Martone Editorial Responsibility: C. Pfister (Associate Editor) 2018). Medullary cells along the transition zone 1367 1368 LAURAN M. LIGGAN ET AL. begin tearing, releasing gas into the newly opened mechanisms that give rise to different gases within space (Dromgoole 1981a). pneumatocysts and determined if gas composition Pneumatocyst walls are thick and composed of changed throughout sporophyte development. We tissues that are specialized in resisting compres- hypothesized that O2 and CO2 concentrations were sion, preventing pneumatocysts from buckling influenced by pneumatocyst SA:V such that gas con- under hydrostatic pressure (Liggan and Martone centrations (% or ppm) and the amount of gas pro- 2018). In addition, pneumatocysts have internal duced (mmol) would decrease (relative to increases pressures that are always less than atmospheric in volume) as pneumatocysts grow. We assumed that pressure, which maintains a positive pressure gra- CO is purely a product of early pneumatocyst devel- dient and keeps the walls under compression as opment, and hypothesized that concentrations of they rise toward the surface (Liggan and Martone CO would initially increase as medulla tissue tears 2018). As pneumatocysts continue to grow and (roughly proportional to pneumatocyst length), but enlarge more than two orders of magnitude in ultimately decrease when cellular division primarily volume, internal pressure stays remarkably con- expands the growing pneumatocyst. stant (Liggan and Martone 2018). Because pneu- Nereocystis thalli (n = 29) of varying pneumatocyst matocyst development involves the active growth volume (5–725 mL) were haphazardly collected of some cells and the degradation of others between April and August 2015 at four sites off the (Dromgoole 1981a), it is unknown which gases fill coast of British Columbia, Canada: Scott’s Bay this newly opened space and which cells con- (48°50004.9″ N 125°08050.0″ W), Aguilar Point tribute to gas composition. In addition, it is (48°50022.0″ N 125°08027.2″ W), Stanley Park unclear whether changes in pneumatocyst size and (49°18003.5″ N 123°07000.0″ W), and Helby Island corresponding physiological processes influence (48°51019.6″ N 125°10007.4″ W). Kelp were collected internal gas composition and concentration. no deeper than 2 m below chart datum and all sam- Because past studies of Nereocystis pneumatocyst ples were detached from the substratum at the hold- gas composition have limited their examination to fast so that pneumatocysts were fully intact. 12 mL large, mature sporophytes, this study aims to inves- of gas was extracted with a 26-gauge (0.45 mm) nee- tigate ontogenetic changes in gas composition by dle and syringe from each pneumatocyst and stored examining pneumatocysts of varying size. in an Exetainer (Labco Limited 12 mL, Lampeter, There are three main processes that likely con- UK). All Exetainers were vacuum sealed and con- tribute to gas composition as pneumatocysts tained a septum to allow gas to be stored without increase in size. One is cellular physiology, (i.e., air contamination. Exetainers were punctured no photosynthesis and respiration) where every living more than three times to avoid air contamination cell that releases gases into or absorbs gases from and were stored upside down in distilled water to the pneumatocyst contributes to gas concentration further prevent air contamination (Glatzel and Well (Rigg and Swain 1941). If gas composition is 2008, Sturm et al. 2015). Samples were cooled to entirely dependent on the by-products of photosyn- 5°C during transit and in the laboratory prior to gas thesis and respiration, the combined concentration analyses. (% or ppm) of biologically produced gases such as CO2 and CO concentrations were analyzed at O2 and CO2 would be proportional to tissue surface room temperature (in ppm) using a Q-trak indoor area and volume of the pneumatocyst (SA:V). The air quality monitor 7565 (TSI Inc. Shoreview, MN, second process that may influence pneumatocyst USA). Q-trak sensors were calibrated to 50 ppm of gases is cellular degradation, tearing of medulla tis- CO and 447 ppm of CO2 (CO2 in air). Pneumato- sue and the subsequent release of CO, when the cyst samples were analyzed by injecting 0.5 mL of stipe opens during pneumatocyst development gas through the sensor where CO2 and CO concen- (Foreman 1976). Foreman (1976) developed trations were electronically read after the gas sensor hypotheses regarding the biological processes that ran for 45 s, recording a peak concentration. Nitro- influence CO production, suggesting that CO is a gen (N2) was used to flush out any excess air in the by-product of autolytic cell metabolism, which is sensor that would alter measurements. active during pneumatocyst formation, and inher- Neofox probes (Ocean Optics Inc., FL, USA) ently linked to respiration by a requirement of were used to measure O2 concentrations (in %) in energy in the form of ATP (Nicholson 1970, Dun- gas samples extracted from pneumatocysts. Before can 1973, Foreman 1976). If true, then we would each measurement, a 30 mL flask was flushed with expect CO concentrations to decrease post-develop- 100% N2 to evacuate any residual air. 1 mL of gas ment as tearing subsides and pneumatocysts expand was extracted from the Exetainers and was injected from cellular division (Nicholson 1970, Duncan into the flask. Each sample was mixed with the 1973) and we would expect mature pneumatocysts residual N2 using a magnetic stir bar during the to have lower CO concentrations than young, devel- reading.
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