Occurrence of Nitrogen Fixing Cyanobacterium Trichodesmium under Elevated pCO2 Conditions in the Western Bay of Bengal

Shetye, Suhas; Sudhakar, Maruthadu; Jena, Babula; Mohan, Rahul

doi:https://doi.org/10.1155/2013/350465

International Journal of Oceanography

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Abstract Introduction Results and Discussion Conclusion Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2013 | Article ID 350465 | https://doi.org/10.1155/2013/350465

Occurrence of Nitrogen Fixing Cyanobacterium Trichodesmium under Elevated pCO₂ Conditions in the Western Bay of Bengal

Suhas Shetye,¹Maruthadu Sudhakar,²Babula Jena,¹and Rahul Mohan¹

Academic Editor: Lakshmi Kantha

Received06 Mar 2013

Revised09 Jun 2013

Accepted15 Jun 2013

Published22 Jul 2013

Abstract

Recent studies on the diazotrophic cyanobacterium Trichodesmium showed that increasing CO₂ partial pressure (pCO₂) enhances N₂ fixation and growth. We studied the in situ and satellite-derived environmental parameters within and outside a Trichodesmium bloom in the western coastal Bay of Bengal (BoB) during the spring intermonsoon 2009. Here we show that the single most important nitrogen fixer in today’s ocean, Trichodesmium erythraeum, is strongly abundant in high (≥300 μatm) pCO₂ concentrations. N : P ratios almost doubled (~10) at high pCO₂ region. This could enhance the productivity of N-limited BoB and increase the biological carbon sequestration. We also report presence of an oxygen minimum zone at Thamnapatnam. Earlier studies have been carried out using lab cultures, showing the increase in growth rate of T. erythraeum under elevated pCO₂ conditions, but to our knowledge, this study is the first to report that in natural environment also T. erythraeum prefers blooming in high pCO₂ concentrations. The observed CO₂ sensitivity of T. erythraeum could thereby provide a strong negative feedback to rising atmospheric CO₂ but would also drive towards phosphorus limitation in a future high CO₂ world.

1. Introduction

Climate change will significantly alter the marine environment within the next century and beyond. Future scenarios predict an increase from the current ~380 to ~750 to ~1,000 ppm CO₂ in the atmosphere towards the end of this century [1, 2]. As the ocean takes up this anthropogenic CO₂, dissolved inorganic carbon (DIC) in the surface ocean increases, while the pH decreases [3]. Rising global temperatures are likely to increase the surface ocean stratification, which may affect the light regime in the upper mixed layer as well as nutrient input from deeper waters [4]. Uncertainties remain regarding both the magnitude of the physicochemical changes and the biological responses of organisms, including species and populations of the oceanic primary producers at the base of the food web. In view of potential ecological implications and feedbacks on climate, several studies have examined the sensitivity of key phytoplankton species to pCO₂ [5–8]. Significant response to elevated pCO₂ was observed in N₂-fixing cyanobacteria [9–13], which play a vital role in marine ecosystems by providing a new source of biologically available nitrogen to the otherwise nitrogen-limited regions [14].

Trichodesmium, a colony-forming cyanobacterium, fixes nitrogen in an area corresponding to almost half of Earth’s surface [15] and is estimated to account for more than half of the new production in parts of the oligotrophic tropical and subtropical oceans [16, 17]. Future expansion of the oligotrophic subtropical provinces to higher latitudes due to surface ocean warming and increased stratification is expected to change the spatial extent of Trichodesmium and hence the magnitude of global N₂ fixation by this organism [18]. Recent studies focused on the impact of different environmental factors on the Trichodesmium species which has high abundance and forms massive blooms in tropical and subtropical areas [16, 17]. Higher pCO₂ levels stimulated growth, biomass production, and N₂ fixation [10, 11, 13] and affected the inorganic carbon acquisition of the cells [13]. While elevated sea surface temperatures are predicted to shift the spatial distribution of Trichodesmium species toward higher latitudes [18], the combined effects of pCO₂ and temperature may favour this species and increase its spatial extent even farther [10, 19]. An increase in the average light intensity, caused by the predicted shoaling of the upper mixed layer, may further stimulate photosynthesis and thus growth and N₂ fixation of Trichodesmium [20].

To test the hypothesis that Trichodesmium grows better in elevated pCO₂ conditions, we have carried out field studies within and around the Trichodesmium bloom in the western Bay of Bengal (BoB). In the northern Indian Ocean, studies on Trichodesmium bloom have been mostly in the Arabian Sea [21, 22], but N₂ fixation is a much more important source of nitrogen in BoB than in the Arabian Sea. The Bay is devoid of nutrient supply due to strong stratification, despite the nutrient supply through the rivers [23]. Satellite datasets on chlorophyll a (chl a), sea surface temperature (SST), wind stress (), and sea surface height anomaly (SSHA) were used to observe the spatial extent of bloom and to study the physical processes associated with it.

2. Methodology

2.1. In Situ Observations

Vertical profiles of CTD were collected from six different coastal regions along the east coast of India (Figure 1). At each region, 5 stations were collected based upon the water depth (50, 100, 200, 500, and 1000 m). Seawater samples were collected using a Rosette sampler with 5 litre Niskin bottles mounted on the CTD assembly. Salinity was measured with the help of an Autosal. Nutrients (silicate, phosphate, nitrate, and nitrite) were measured with a Skalar Autoanalyzer by standard colorimetric methods. Standards were used to calibrate the auto analyzer, and frequent baseline checks were made. The standard deviation for duplicates was 0.07 μM for silicate, 0.06 μM for nitrate, and 0.01 μM for nitrite and phosphate. Total carbon dioxide (TCO₂) content of seawater samples was determined using a coulometer (model 5014 of U.I.C. Inc., USA). The reliability of the coulometric titration was regularly checked with certified referenced materials (CRMs, Batch number 92) provided by A. Dickson (SIO, University of California). The accuracy estimated from the CRMs values was 2 μmol for TCO₂. The pH_T and pH_f were measured at 25°C by cresol red spectrophotometry [24]. The pH_T of the samples was then corrected to the in situ temperature following equation of Gieskes [25]. Analytical precision was ~0.002 for pH. In situ pCO₂ was calculated using the dissociation constants of Dickson and Millero [26].

The CO₂ exchange flux (mmol C m⁻² day⁻¹) across the sea-air interface was calculated using equation given in Wanninkhof [27]. , where is the gas transfer velocity, is the solubility of CO₂ gas in seawater [28], and is the difference between surface seawater and atmospheric pCO₂. The sea-air pCO₂ difference is computed using the measured surface water pCO₂ values and the atmospheric pCO₂ from the zonal mean CO₂ concentrations reported by the GLOBALVIEW-CO₂ (2009).

Water samples were collected from patches of Trichodesmium blooms near the coastal Thamnapatnam (in Tamil Nadu, India) and then fixed in a 2% formalin solution to permit the identification and counting of phytoplankton. Samples fixed in formalin were observed through a polarising microscope for species identification.

2.2. Satellite-Derived Environmental Parameters

Satellite observations were used to study the spatial extent of bloom and the physical processes associated with it. SeaWiFS (Sea-viewing Wide Field-of-view Sensor) based Level-3 global standard mapped images (SMI) of climatological chl values (9 km spatial resolution) were acquired from Goddard Space Flight Centre (GSFC), for the month of May (1997–2010). Chl datasets based upon SeaWiFS operational bio-optical algorithm (i.e., ocean color, OC4) developed by O’Reilly et al. [29] and later updated (OC4v6) by National Aeronautics and Space Administration (NASA) Ocean Biology Processing Group (OBPG). The previous algorithm yields a strong correlation () with in situ Chl on global scale that includes samples from all water types [29]. Level-3 Pathfinder SSTs dataset (4 km spatial resolution) from the Advanced Very High Resolution Radiometer (AVHRR) was obtained from NASA’s Jet Propulsion Laboratory (JPL) and utilized during the bloom period. Multiple satellite altimeters (Jason-1, TOPEX/Poseidon, ERS 1/2, and GFO) merged product on sea surface height anomalies (SSHA) at a spatial resolution of were obtained from the NASA Physical Oceanography Distributed Active Archive Center (PODAAC). QuikScat-measured wind vector (scalar wind speed with corresponding and components) data files available at spatial resolution of 25 km were downloaded from http://www.ssmi.com/. The wind stress () was then calculated using variable drag coefficients () given by Yelland and Taylor [30].

3. Results and Discussion

3.1. Observed Variability of Physicochemical Parameters

BoB is highly influenced by monsoons and receives large volume of freshwater from both river discharge and rainfall [31, 32] which results in low sea surface salinity (SSS). All stations had salinity < 34 and temperature > 29°C except Thamnapatnam. At Thamnapatnam surface salinity was 34.53, and the SST was 27.2°C.

Depth profiles of SST, SSS, and nutrients (NO₃, NO₂, PO₄, and SiO₄) are shown in Figure 2. Surface NO₃ concentrations were <1 μM up to 75 m depth at all stations except Thamnapatnam, where it reached concentrations of 13 μM at 20 m and went on increasing with depth. SiO₄ concentrations were <5 μM up to 20 m at all stations except Thamnapatnam. Phosphate concentrations also were <0.5 μM in surface waters, except Thamnapatnam. Dissolved oxygen concentrations were high at the surface and were above 4 mL/L at all stations. Maximum concentration was found at Chennai, reaching up to 5.89 mL/L (Figure 2). Concentration decreased rapidly with depth, and an intense oxygen minimum zone (OMZ) is seen between 150 and 500 m. At Thamnapatnam the OMZ starts from 75 m. Surface pH was greater than 8.3 at all stations and decreased with depth. was less than 300 uatm at all stations except Thamnapatnam, where the maximum was 376 uatm (Figure 3). The average CO₂ flux in Bay of Bengal was −12.8 mmol C m⁻² day⁻¹, whereas at Thamnapatnam the CO₂ flux was −3.9 mmol C m⁻² day⁻¹ (Figure 3). The negative sign indicates that the region is a sink for atmospheric CO₂.

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

3.2. Physical Forcing

The shoaling of thermocline, halocline, nutricline, and elevated CO₂ and oxygen deficient water (Figure 2) near 14°N (off Thamnapatnam) is due to shoaling and resulted from divergence of water masses. The shoaling-induced cooling feature is well captured by NOAA AVHRR derived SST during May 12, 2009 (Figure 4(a)) and also reflecting in weekly composite product (9–16th May 2009) signifying persistency of the feature (Figure 1). Satellite observations indicated lower SST (~27°C to ~27.5°C) and associated negative SSHA ranging from −0.1 m to −0.2 m near the bloom region off Thamnapatnam (Figures 4(a) and 4(b)). These features represent an upwelling area where cold, high nutrient, and dense waters are pushed to the surface (Figure 2), leading to phytoplankton bloom. The alongshore wind stress is favourable off Thamnapatnam to induce coastal upwelling finally resulting in a phytoplankton bloom (Figure 4(c)).

(a)

(b)

(c)

3.3. Distribution of Trichodesmium erythraeum

Colonies of the cyanobacterium (1-2 mm size bundles of trichomes) could be seen with the naked eye in the surface water at all stations along Thamnapatnam. At Thamnapatnam stations, surface water was blooming with this cyanobacterium, possibly the dominant primary producer during this period. Analysis of the surface plankton collections revealed the presence of Trichodesmium erythraeum in the sample. It appeared that T. erythraeum was concentrated in the upper 3 meters of the water column due to its positive buoyancy [33–35] and the surface water attained a brownish color. Around 4500 filaments of T. erythraeum per litre seawater were observed. A colony of T. erythraeum collected from the Thamnapatnam consisted of cells. T. erythraeum comprised 100% of total cell count and showed complete dominance over other phytoplankton.

The T. erythraeum bloom reported here assumes considerable importance as the BoB is believed to be a region of relatively low productivity compared to the Arabian Sea. Stratification caused by freshwater influx is thought to restrict upwelling of nutrients. Stratification in the southern BoB is weaker than in the north [36, 37].

During spring intermonsoon, eddies and recirculation zones from the coastal regions of BoB due to the western BoB current (WBC) were found to enhance phytoplankton growth [38, 39]. Since the chl in the upper layer of BoB is limited by the availability of nutrients, such oceanic processes that can bring nutrients into the euphotic zone are of prime importance. Nutrients are brought to surface waters by coastal upwelling driven by alongshore winds (Figure 4(c)). In order to identify the physical process that could cause the high chl blooms described previously, we have examined the relevant physicochemical oceanographic data, and the results corresponding to May 12, 2009 are shown in Figure 2. The winds have a large alongshore component (Figure 4(c)) and strong offshore component, thus resulting in coastal upwelling.

Since the surface water temperature was >26°C, it would have favored the Trichodesmium bloom as marine cyanobacteria exhibit temperature optima somewhere in the range of 25–35°C [40]. Studies by Suvapepun [41] and Sellner [42] have reported that cyanobacteria require higher temperature optima for growth than other phytoplankton and that the temperature has been the most important factor contributing to cyanobacterial dominance. Buoyancy regulation by cyanobacteria plays a key role in this phenomenon, as soon as the wind abates; cyanobacteria float rapidly towards the surface due to their positive buoyancy [42]. The surface accumulations are quickly dispersed over the water column by wind-induced mixing at wind speeds over 6–8 m s⁻¹ [43].

While effects of CO₂-related seawater acidification have been demonstrated for a variety of marine microalgae and cyanobacteria [44], mainly focusing on carbon acquisition and concentrating mechanisms [45], little is known about its impact on marine diazotrophs. Earlier studies by Hutchins et al. [10], Ramos et al. [9], Levitan et al. [11], and Kranz et al. [13] reported from lab experiments that T. erythraeum prefers high CO₂ conditions. This trend is predominantly attributed to changes in cell division [10, 11] but also altered elemental ratios of carbon to nitrogen [11] or nitrogen to phosphorus [9]. A first step toward a mechanistic understanding of responses in T. erythraeum has been taken by Levitan et al. [11], focusing on pCO₂ dependency of nitrogenase activity and photosynthesis. We tried to investigate the same hypothesis in natural environment, and we found T. erythraeum blooms at Thamnapatnam station which had the highest pCO₂ concentrations. At Thamnapatnam all the 5 stations had pCO₂ concentrations ≥ 300 μatm. In T. erythraeum, photosynthetically generated energy (ATP and NADPH) is primarily used for the fixation of CO₂ in the Calvin-Benson cycle. Cyanobacterial Rubisco possesses one of the lowest CO₂ affinities among phytoplankton [46], their Rubisco is confined to multiple capsid-like carboxysomes and helps to minimize CO₂ leakage [47] thus giving them advantage over other phytoplankton groups.

Nitrogen fixation by Trichodesmium also alters the N : P ratio and could drive towards phosphate limitation. N : P ratio was 10 at Thamnapatnam, whereas in Chennai it was 5.3, clearly indicating phosphorus limitation in Trichodesmium blooms. The average N/P ratio upto 200 m at all stations was less than 10, indicating large deviations from the standard Redfield’s N/P ratio of 16. Analysis of climatological SeaWiFS chlorophyll a image for the month of May off Thamnapatnam (Figure 5) indicated elevated chl a concentration up to ~3 mg/m³. Jyotibabu et al. [48] have reported primary productivity as high as 2160 mg C m⁻² d⁻¹ with in the bloom in BoB.

Upwelling brought high pCO₂ water and nutrients from subsurface to surface and led to blooming of Trichodesmium at surface. The underlying processes responsible for the strong CO₂ sensitivity in this important diazotroph are currently unknown. Our results clearly indicate that with rise in CO₂ in future, the abundance of Trichodesmium sp. and N₂ fixation could have potential biogeochemical implications, as it may stimulate productivity in N-limited oligotrophic regions and thus provide a negative feedback on rising atmospheric CO₂ levels.

4. Conclusion

This study has been carried out by conjunctive analysis of in situ and satellite observations within and outside a Trichodesmium bloom in the western Bay of Bengal during the spring intermonsoon 2009. Oceanic environmental parameters such as SST, chl a, wind, and SSHA measured from remote sensing satellites are useful to study the bloom due to its synoptic, high spatial resolution, and repetitive characteristics. In this study we show that Trichodesmium is strongly abundant in high pCO₂ (>300 μatm) concentrations. N : P ratios almost doubled (~10) at this high CO₂ region. We also report presence of an oxygen minimum zone in the Bay of Bengal. Earlier studies have been carried out using lab cultures, showing the increase in growth rate of Trichodesmium in high pCO₂ conditions, but our study proves for the first time that in natural environment also Trichodesmium bloom in high pCO₂ waters. The observed CO₂ sensitivity of Trichodesmium could thereby provide a strong negative feedback to rising atmospheric CO₂ but could also lead towards phosphate limitation. Our study also proves that Thamnapatnam is a site for coastal upwelling, OMZ, and Trichodesmium bloom formation. However, metabolic processes must be studied in detail to understand the responses of Trichodesmium to changes in environmental conditions.

Acknowledgments

The authors would like to thank the Ministry of Earth Sciences for providing the necessary ship time. The authors thank the captain, crew, participants, and technical staff of the FORV Sagar Sampada for their invaluable assistance. The authors also thank the chief scientist Dr. Rosamma Philip for her support. SeaWiFS dataset was provided by NASA’s Goddard Space Flight Center. The AVHRR and QuikScat data were obtained from the NASA Physical Oceanography Distributed Active Archive Center (PODAAC).

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Copyright © 2013 Suhas Shetye et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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