In order to prevent salt damage because seaweed enzymes can only operate under hypohaline conditions (salinity ≈ 6‰ - 12‰) but also obtain for photosynthesis an in the aquatic environment—due to a 10,000 fold strongly limited carbon source—seaweeds developed several mechanisms to meet these vital demands for survival in the harsh euhaline oceanic environment (salinity range: 32‰ - 35‰), we tested this range of adaptation mechanisms in the euhaline oceanic collected water in combination with the seaweed moisture. We obtained under laboratory conditions at 10 bar mechanical pressure for four seaweed species: Ulva lactuca, Caulerpa sertularioides, Caulerpa cf. brachypus (all three green) and Undaria pinnatifidia (brown). Oceanic water and seaweed moisture were measured for salinity, pH and by Inductively Coupled Plasma Spectroscopy (ICP)-techniques concentrations for macro-elements: (Ca, Fe, K, Mg, Mn, Na, P, & S), micro-elements ≈ [HM]: (Al, As, Cd, Co, Cr, Cu, Mo, Ni, Pb & Zn) and nutrients (N-total & P-total). The [seawater compound X]/[oceanic compound X] ration is a reflection of an inward (uptake) or excretion mechanism over the seaweed cellular membrane which is operative. Our observations gave a clear dispersion to salinity stress with on one hand the green seaweed U. lactuca and on the other the brown seaweed U. pinnatifidia. Both Caulerpa spp. took in an intermediate position. Observed in compensatory responses to salinity stress was ranging Ulva sp. both Caulerpa spp.-Undaria sp.: 1) amount pressed seaweed moisture: [ml/g Fresh Weight]; 2) salinity: (in ‰); 3) Na+ storage vacuole volume; 4) Na+:K+ ratio (reflection of K+ as osmolyticum); 5) ∑[HM] (as osmolyticum); 6) pH (seaweed moisture); 7) Nutrients (N & P); 8) availability of essential metal elements for plants (Cu, Fe, Zn, Mn, Mo, Ni); 9) transport direction of micro- and macro-elements. Finally, the role of brown vs. green seaweeds in the evolutionary eukaryotic tree of life in relation to the ability of the brown seaweeds to produce their own osmolyticum will be discussed.
At present, terrestrial agriculture is at its limits mainly for available land area and fertilizers (reviewed: [
This shift “towards a seaweed-based economy” [
In this research we will focus on the salt extrusion mechanism of the seaweeds, without an efficient aquatic photosynthesis which would be impossible [
supporting biological reactions as co-factors for numerous vital enzymes. Therefore, the uptake and assimilation of K+ are imperative for overall plant health and growth. However, Na+ competes with K+ for intracellular influx, such that many K+ transport systems tend to also have high affinities for Na+ and thus function as Na+/K+ symporters [
Seaweed Species | Na+ (mg∙g−1) | K+ (mg∙g−1) | [Na+: K+] | Tissue type | Salinity (euhaline#) | Reference |
---|---|---|---|---|---|---|
Chondrus crispus | 42.7 | 31.8 | 2.28 | Whole plant | Seawater | [ |
Fucus vesiculosus | 54.7 | 43.2 | 2.15 | Whole Plant | Seawater | [ |
Laminaria digitata | 38.2 | 115.8 | 0.56 | Whole plant | Seawater | [ |
Porphyra tenera | 36.3 | 35.0 | 1.77 | Whole plant | Seawater | [ |
Sargassum mangarevense | 14.6 | 70.2 | 0.35 | Whole plant | Seawater | [ |
Turbinaria ornate | 19.3 | 112.2 | 0.29 | Whole plant | Seawater | [ |
Undaria pinnatifida | 70.6 | 86.9 | 1.38 | Whole plant | Seawater | [ |
Mean ± STD | 39.5 ± 7.3 | 70.7 ± 13.4 | 1.25 ± 0.32 |
environment as kind of osmolyticum [Note: the Na+ & K+ composition of seawater is respectively 19.3 and 0.4 mg∙ml−1 at 35 psu respectively which gives an [Na+:K+] ration of ≈48.25 [
In the review article of [
Seaweeds:
− Ulva lactuca (Chlorophyta): Katse Heule, Eastern Scheldt, The Netherlands; approximate coordinates: 51˚32'30 N and 3˚52'E.
− Caulerpa sertularioides (Chlorophyta): purchased by Burgers’ Zoo, Arnhem, (the Netherlands) Origin: Denpassar, Bali, Indonesia: approximate coordinates: 8˚41'S and 115˚17'E.
− Caulerpa cf. brachypus (Chlorophyta): was obtained from “De Jong Marinelife”, Spijk, (The Netherlands) Origin: Havanna, Cuba: approximate coordinates: 23˚50'S and 82˚50'W.
− Undaria pinnatifidia (Wakame) (Phaeocophycea): Kilcar, West Donegal, Ireland, approximate coordinates: 54˚37'N and 8˚37'W.
While seaweeds were collected, a water sample of the surrounding oceanic water was sampled at the same time stored at −80˚C pending analysis.
Sampling of four seaweeds including surrounding oceanic water was performed during the months June-September in the year 2016.
Dry weight seaweeds:
After collection, the seaweeds were brought as soon as possible to the laboratory. Most epiphytic material was removed; the seaweeds were rinsed quickly with freshwater, air-dried, oven-dried (one night at 60˚C and one night at 105˚C), weighed and the dry matter content calculated.
Experimental set up:
In this experiment we determined for four seaweed species under mechanical pressure until 10 barr (see further) the percentage of moisture weight. Also the dry weight of the seaweeds was determined in an oven overnight (see above) In the freshly collected seaweed moisture we determined directly the salinity (in ‰) and the osmolarity (EC-value) expressed in [mS/cm]. Also the pH of oceanic water and seaweed moisture were determined with a PHH-7011 pH meter with automatic temperature compensation (Omega, the Netherlands) Thereafter the obtained seaweed moisture was immediately stored at −80˚C pending analysis of micro- & macro-elements. Microelements ≈ heavy-metals = [HM], (Al, As, Cd, Co, Cr, Cu, Mo, Ni, Pb & Zn) and macro-elements (Ca, Fe, K, Mg, Mn, Na, P, & S) were measured by Inductively Coupled Plasma Spectroscopy (ICP) techniques at the central Chemical Biological Laboratory for Soil & Water Research at Wageningen University (details see further) The earlier mentioned simultaneously with the seaweeds sampled oceanic water was directly deep frozen but now in conjunction with the samples of the seaweeds in a similar way ICP analyzed. This approach justifies a simultaneously comparison of [micro-] & [macroelements] of both compartments (seaweed moisture versus oceanic water). From these laboratory measurements we calculated parameters which might be important in elucidating the complex sodium extrusion mechanism of the four investigated seaweeds.
Mechanical pressure procedure: To be able to produce press moisture from the seaweeds, the plant material (300 - 1000 g) was first pulped using a laboratory homogenizer (manufacturer: Foss Tecator, type: Tecator 1094 Homogenizer,), with either a smooth or a serrated knife, at s speed of 1500 rpm or 3000 rpm. Moisture was pressed out of the pulp, approximately 100 g of pulp was used, using a LLOYD INSTRUMENTS (type: LR30K) testing machine that was fitted with a specially constructed unit for pressing pulps at a maximum pressure of 60 bar. Final weight of press cake and press moisture was determined. Afterwards press cake and samples of the obtained seaweed moisture of the four different seaweed species (n = 4 per seaweed species) were immediately stored at −80˚C pending analyses.
Determination of micro- and macro-elements by Inductively Coupled Plasma spectroscopy (ICP-techniques):
1) Al, As, Ca, Cd, Cr, Cu, Fe, K, Mg, Mn, Na, Ni, P, Pb, S and Zn in seaweed moisture and in the sample of the surrounding waters were measured on an ICP-AES (Thermo Iris) according pretreatment SWV E-3404, measurement SWV E-1304 and conservation SWV E-3404 guide lines at the Chemical Biological Laboratory for Soil & Water Research, Wageningen University, Wageningen (The Netherlands).
2) As, B, Ba, Cd, Co, Cr, Cu, La, Li, Mn, Mo, Ni, Pb, Sb, Se, Sn, and V in seaweed moisture and in the sample of the surrounding waters were measured on an HR-ICP-MS (Thermo Element 2) according pretreatment SWV E-3404, measurement SWV E-1325 and conservation SWV E-3404 guidelines at the same laboratory.
Salinity & pH measurements: Salinity of the seaweed moisture and oceanic water were determined using an EC meter (manufacturer: WTW; type Cond 315i/SET) fitted with a conductivity cell (manufacturer: WTW; type: TetraCon 325, cell constant 0.475 cm−1). The pH of seaweed moisture and oceanic water were determined with a PHH-7011 pH meter with automatic temperature compensation (Omega, the Netherlands).
Classification salinity:
Classification in a certain salt range and terminology will be based on the ( [
N-total and P-total measurements: N-total and N-NH4 measurement were performed on a Segmented Flow Analyzer (SFA) apparatus according to SWV E1417 guide lines at the Chemical Biological Laboratory for Soil Research, Wageningen University, Wageningen (The Netherlands) Determination of P3 was performed on an HR-ICP-MS (Thermo Element-2) according pretreatment SWV E-3404, measurement SWV E-1325 and conservation SWV E-3404 guide lines at the same laboratory.
Zone | Salinity range (in ‰) |
---|---|
Limnetic | <0.5 |
β-Oligohaline | 0.5 - 3 |
α-Oligohaline | 3 - 5 |
β-Mesohaline | 5 - 10 |
α-Mesohaline | 10 - 18 |
Polymixohaline | 18 - 30 |
Euhaline | 30 - 40 |
Hyperhaline | >40 |
Salinity content water | mg/l TDS | Definition | Salinity in ‰ |
---|---|---|---|
Drinking water | 500 | Consumption water | 0.5‰ |
Fresh water | Less than 1000 | Fresh water | =1‰ |
Slightly saline | 1000 to 3000 | Brackish water | 1‰ - 3‰ |
Moderately saline | 3000 to 10,000 | Brackish water | 3‰ - 10‰ |
Highly saline | Over 10,000 | Brackish water | >10‰ |
Oceanic water | 35,000 | Marine water | 35‰ |
Calculations:
1) pH = − log 10 H + ⇔ [ H + ] = 10 − pH [ mol / l ] [
pH-value and from this value calculated according to 10pH the amount of H+-ions in (mol/l) was calculated [
2) Accumulation factor = Heavy-metal ( HM ) in the seaweed moisture Heavy-metal ( HM ) in the oceanic water
3) Na + / K + ratio = Na + ( mg / l ) / K + ( mg / l )
Weights and Volumes:
The following weights and volumes were obtained from the overnight oven-dried seaweed material and the 10 bar mechanical pressed fresh seaweed biomass:
*Oven-dried:
4) DryWeight [ g ] = W-tray oven dried material [ g ] − W-empty tray [ g ] W-tray with fresh material [ g ] − W-empty tray [ g ]
*Mechanical Pressure:
5) Total Moisture Weight [g] = (Weight pressed moisture [g]) + (Losses moisture in machine [g]).
6) With: Losses moisture in the machine = (Wpulp [g] − Wpress moisture [g] − Wpress cake [g]).
7) With: W = Weight in gram [g].
*Vacuole size cell:
Based on the following three assumptions that:
1) The whole seaweed cell vacuole is 100 % filled with seaweed moisture (see
2) At the applied 10 bar mechanical pressure procedure the whole volume of the seaweed cell vacuole will be squeezed empty;
3) 1 ml seaweed moisture will weight 1 gram and has with a corresponding specific gravity of water a volume of one cubic cm.
We will conclude that the calculated “Total Moisture Weight” in (g) will correspond to the volume of the seaweed cell vacuole.
In
Seaweed spp. | Lab No | Calculated Dry matter. DW in (g) | Calcul. Total moist. WW in (g) | WW/DW | lab salinity prom. | lab EC mS/cm | lab pH mg/l | Lab Na+ mg/l | Seaweed ∑[HM] mg/l | Ocean ∑[HM] mg/l | Lab P-tot mg/l |
---|---|---|---|---|---|---|---|---|---|---|---|
Ulva | Zs1 | 9.37 | 47.19 | 5.04 | 9.60 | 14.77 | 5.08 | 40.90 | 94.20 | 420.00 | 88.90 |
lact. | Zs2 | 9.56 | 48.29 | 5.05 | 9.40 | 14.47 | 5.30 | 45.80 | 93.40 | 432.00 | 91.40 |
NL | Zs3 | 9.36 | 45.52 | 4.86 | 9.40 | 14.38 | 4.94 | 42.70 | 90.60 | 360.00 | 83.10 |
Zs4 | 9.24 | 44.80 | 4.85 | 9.60 | 13.68 | 4.93 | 42.90 | 87.60 | 359.00 | 85.30 | |
Mean | 9.38 | 46.45 | 4.95 | 9.50 | 14.33 | 5.06 | 43.08 | 91.45 | 392.75 | 87.18 | |
Std. | 0.14 | 1.58 | 0.11 | 0.12 | 0.46 | 0.17 | 2.03 | 2.99 | 38.71 | 3.69 | |
Caul. | Cs1 | 1.39 | 71.94 | 51.94 | 19.10 | 27.80 | 4.17 | 4.81 | 37.30 | 362.00 | 45.00 |
sert. | Cs2 | 1.29 | 70.17 | 54.40 | 19.50 | 28.30 | 4.20 | 4.61 | 38.20 | 344.00 | 45.00 |
Bali | Cs3 | 1.25 | 86.86 | 69.66 | 19.50 | 28.30 | 4.20 | 4.62 | 37.60 | 348.00 | 44.80 |
Cs4 | 1.21 | 76.32 | 62.92 | 19.30 | 28.20 | 4.20 | 4.71 | 37.50 | 351.00 | 45.20 | |
Mean | 1.28 | 76.32 | 59.73 | 19.35 | 28.15 | 4.19 | 4.69 | 37.65 | 351.25 | 45.00 | |
Std. | 0.07 | 7.49 | 8.12 | 0.19 | 0.24 | 0.02 | 0.09 | 0.39 | 7.72 | 0.16 | |
Caul. | Ci-1 | 1.19 | 50.23 | 42.39 | 20.50 | 29.70 | 4.51 | 14.40 | 369.00 | 922.00 | 91.40 |
brach. | Ci-2 | 1.25 | 52.05 | 41.54 | 20.60 | 29.70 | 4.51 | 14.50 | 374.00 | 917.00 | 92.80 |
Cuba | Ci-3 | 1.13 | 57.47 | 50.81 | 20.70 | 29.90 | 4.50 | 14.60 | 377.00 | 920.00 | 92.50 |
Ci-4 | 1.17 | 53.25 | 45.40 | 20.50 | 29.80 | 4.51 | 14.70 | 374.00 | 917.00 | 93.40 | |
Mean | 1.19 | 53.25 | 45.03 | 20.58 | 29.78 | 4.51 | 14.55 | 373.50 | 919.00 | 92.53 | |
Std. | 0.05 | 3.08 | 4.19 | 0.10 | 0.10 | 0.00 | 0.13 | 3.32 | 2.45 | 0.84 | |
Undar | Wa1 | 28.41 | 39.88 | 1.40 | 9.60 | n.d. | 6.53 | 14.60 | 0.00 | 123.00 | 17.80 |
Pinnat | Wa2 | 28.74 | 62.70 | 2.18 | 9.80 | n.d. | 6.44 | 10.10 | 0.00 | 96.60 | 12.60 |
IR | Wa3 | 27.22 | 83.03 | 3.05 | 9.80 | n.d. | 6.50 | 8.27 | 0.00 | 91.20 | 11.60 |
Wa4 | 28.15 | 79.29 | 2.82 | 5.90 | n.d. | 6.57 | 5.92 | 0.00 | 83.10 | 10.60 | |
Mean | 28.13 | 66.22 | 2.36 | 8.78 | n.d. | 6.51 | 9.72 | 0.00 | 98.48 | 13.15 | |
Std. | 0.65 | 19.66 | 0.74 | 1.92 | n.d. | 0.05 | 3.67 | 0.00 | 17.27 | 3.21 |
In
When considering the composition of Na+ and K+ in seawater (19.3 mg∙ml−1 and 0.4 mg∙ml−1 at 35 psu, respectively gives in this case an Na+/K+ ratio of 48.25 seawater of [
Location Ocean | Na+ (mean) | K+ (mean) | Na+/K+ (mean) | Seaweed species | Na+ (mean) | K+ (mean) | Na+/K+ (mean) |
---|---|---|---|---|---|---|---|
Netherlands | 9983 | 321 | 31.1 | Ulva lactuca | 1363.0 | 1205.0 | 1.13 |
Indonesia | 10020 | 384 | 26.1 | Caulerpa sert. | 6238.8 | 481.0 | 12.97 |
Cuba | 10840 | 361 | 30.0 | Caulerpa brach. | 6678.5 | 675.5 | 9.89 |
Ireland | 18230 | 547 | 33.3 | Undaria pinnat. | 3147.0 | 121.3 | 25.94 |
clear that mechanisms must be in place to minimize cytosolic Na+ accumulation while permitting necessary K+ uptake. The dissimilarity between Na+ and K+ concentrations in seawater at all four oceanic locations is ≈30 with of course [K+] ≈ 30 fold lower. The [Na+:K+] molar ratio of our seaweeds was the lowest in the seaweed Ulva lactuca ≈ 1.13 which is indicative that K+ is in this green seaweed species acting as an important osmolyticum. The two Caulerpa spp. Are in the intermediate range of around ≈11.5 (range 9.9 - 13.0), while in the brown seaweed Undaria pinnatifidia this value is around 26. For the latter species this implies that K+ has no important role as major osmolyticum and give strong evidence that this brown seaweed is able to produce biochemically its own osmolyticum. In general, brown seaweeds are able to produce a large variation of economically important osmolyticuma. In general, these by brown seaweeds produced osmolyticuma are or from the carbohydrate fraction or phycocolloid fraction. Although we didn’t measure any osmolyticum of one of these fractions in Undaria pinnatifidia this extremely high [Na+:K+] molar ratio of ≈26 gives strongly evidence that this species is able to produce its own osmolyticum.
The moisture of seaweeds has a rather low salinity (brackish) in order of descending salinity (mean ± std (n = 4) in ‰): Caulerpa cf. brachypus ≈ 20.58 ± 0.096 (Polymixohaline); Caulerpa sertularioides ≈ 19.30 ± 0.163 (Polymixohaline); Ulva lactuca ≈ 9.501 ± 0.115 (β-Mesohaline) and Undaria pinnatifidia ≈ 9.500 ± 0.115 (β-Mesohaline) [
Ulva lactuca had the highest P-content (69.7 mg/l), Undaria pinnatifidia the lowest (13.2 mg/l) while both Caulerpa spp. had an intermediate position. N-NH4 had the highest value in Ulva lactuca (34.5 mg/l) and the lowest in Caulerpa sertlatioides (4.7 mg/l) Interestingly Nts was the highest in Caulerpa cf. brachypus (298.8 mg/l) while was surprisingly zero in Undaria pinnatifidi (Tables 6-8).
Excess salt is toxic for terrestrial plants but also for seaweeds living in the euhalien [
Sample nr. | Seaweed Species | Ca2+ [mg/l] | Fe2+ [mg/l] | K+ [mg/l] | Mg2+ [mg/l] | Mn2+ [mg/l] | Na+ [mg/l] | SUM MACRO CATIONS | P3− [mg/l] | S2− [mg/l] | SUM MACRO ANIONS |
---|---|---|---|---|---|---|---|---|---|---|---|
Threshold | 1.20 | 0.09 | 0.40 | 0.15 | 0.01 | 0.30 | 0.10 | 0.20 | |||
1) | Ulva lactuca | 552.50 | 2.74 | 1205.00 | 1762.00 | 3.77 | 1363.00 | 4889.00 | 87.18 | 5493.25 | 5580.43 |
20.70 | 0.40 | 34.29 | 47.85 | 0.16 | 26.26 | 121.42 | 3.69 | 87.55 | 86.47 | ||
2) | Caulerpa sertlatiodes | 530.00 | 1.08 | 481.00 | 509.25 | 1.18 | 6238.75 | 7761.26 | 45.00 | 581.75 | 626.75 |
25.47 | 0.04 | 5.35 | 9.03 | 0.03 | 92.33 | 115.76 | 0.16 | 155.56 | 155.56 | ||
3) | Caulerpa cf. brach. | 440.00 | 0.90 | 675.50 | 776.00 | 2.05 | 6678.50 | 8572.95 | 92.53 | 1376.50 | 1469.03 |
3.27 | 0.14 | 4.12 | 12.25 | 0.07 | 75.12 | 84.28 | 0.84 | 79.35 | 80.13 | ||
4) | Undaria pinnatifidia | 110.50 | 0.25 | 121.25 | 327.50 | 0.02 | 3147.00 | 3706.52 | 13.15 | 345.50 | 358.65 |
1.00 | 0.03 | 5.32 | 8.66 | 0.01 | 32.32 | 37.79 | 3.21 | 7.19 | 8.67 | ||
Sample nr. | Four Oceans | Ca2+ [mg/l] | Fe2+ [mg/l] | K+ [mg/l] | Mg2+ [mg/l] | Mn2+ [mg/l] | Na+ [mg/l] | SUM MACRO CATIONS | P3− [mg/l] | S2− [mg/l] | SUM MACRO ANIONS |
Threshold | 1.20 | 0.09 | 0.40 | 0.15 | 0.01 | 0.30 | 0.10 | 0.20 | |||
1). | Netherlands | 291.00 | 0.09 | 321.00 | 1214.00 | 0.01 | 9983.00 | 11809.10 | 0.10 | 933.00 | 933.10 |
2). | Indonesia | 313.00 | 0.09 | 384.00 | 1206.00 | 0.01 | 10020.00 | 11923.10 | 0.02 | 866.00 | 866.02 |
3). | Cuba | 334.00 | 0.09 | 361.00 | 1336.00 | 0.01 | 10840.00 | 12871.10 | 0.79 | 983.00 | 983.79 |
4). | Ireland | 473.00 | 0.09 | 547.00 | 2212.00 | 0.01 | 18230.00 | 21462.10 | 0.01 | 1683.00 | 1683.01 |
Mean | 352.75 | 0.09 | 403.25 | 1492.00 | 0.01 | 12268.25 | 14516.35 | 0.23 | 1116.25 | 1116.48 | |
Std | 82.07 | 0.00 | 99.31 | 483.67 | 0.00 | 3994.14 | 4654.91 | 0.38 | 380.86 | 380.75 | |
Sample nr. | Ratio seaweed/ocean | Ca2+ [mg/l] | Fe2+ [mg/l] | K+ [mg/l] | Mg2+ [mg/l] | Mn2+ [mg/l] | Na+ [mg/l] | SUM MACRO CATIONS | P3− [mg/l] | S2− [mg/l] | SUM MACRO ANIONS |
Threshold | 1.20 | 0.09 | 0.40 | 0.15 | 0.01 | 0.30 | 0.10 | 0.20 | |||
1) | Ulva/ocean | 1.90 | 30.39 | 3.75 | 1.45 | 376.75 | 0.14 | 414.38 | 871.75 | 5.89 | 877.64 |
0.07 | 4.48 | 0.11 | 0.04 | 16.07 | 0.00 | 14.50 | 36.94 | 0.09 | 36.92 | ||
2) | Caulerpa sert./ocean | 0.35 | 2.73 | 0.32 | 0.27 | 2.05 | 0.31 | 6.04 | 657.50 | 0.40 | 657.90 |
0.00 | 0.35 | 0.01 | 0.01 | 0.58 | 0.00 | 0.79 | 160.29 | 0.01 | 160.29 | ||
3) | Caulerpa brach./ocean | 0.87 | 1.00 | 0.89 | 0.91 | 1.00 | 0.92 | 5.59 | 0.13 | 0.95 | 1.08 |
0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
4) | Undaria/ocean | 0.66 | 1.00 | 0.70 | 0.55 | 1.00 | 0.55 | 4.46 | 2.00 | 0.51 | 2.51 |
0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 |
Sample nr. | Seaweed Species | Cu2+ [µg/l] | Al3+ [µg/l] | Zn2+ [µg/l] | Cd2+ [µg/l] | Co2+ [µg/l] | Cr3+ [µg/l] | Mo4+ [µg/l] | Ni2+ [µg/l] | Pb2+ [µg/l] | SUM MICRO CATIONS |
---|---|---|---|---|---|---|---|---|---|---|---|
Threshold | 0.10 | 0.30 | 0.30 | 0.01 | 0.01 | 0.02 | 0.18 | 0.03 | 0.04 | ||
1) | Ulva lactuca | 330.75 | 153.00 | 1232.25 | 2.39 | 13.88 | 18.65 | 14.33 | 157.50 | 1.26 | 1924.00 |
74.29 | 20.99 | 236.99 | 0.34 | 0.33 | 0.90 | 1.00 | 9.68 | 1.66 | 271.67 | ||
2) | Caulerpa sertlaiodes | 117.85 | 582.75 | 1169.50 | 5.72 | 6.99 | 14.50 | 6.99 | 129.75 | 2.45 | 2036.49 |
13.23 | 175.55 | 361.52 | 0.47 | 0.21 | 0.39 | 4.61 | 5.32 | 1.53 | 341.40 | ||
3) | Caulerpa cf. brach. | 788.25 | 230.00 | 1136.00 | 4.43 | 22.13 | 20.23 | 8.54 | 295.25 | 1.33 | 2506.15 |
69.21 | 46.45 | 146.50 | 0.22 | 0.22 | 1.25 | 0.35 | 9.36 | 0.95 | 257.38 | ||
4) | Undaria pinnatifidia | 73.90 | 156.00 | 178.75 | 0.81 | 1.04 | 6.16 | 14.80 | 20.08 | 0.09 | 451.63 |
12.78 | 9.93 | 18.45 | 0.13 | 0.12 | 0.27 | 3.00 | 3.89 | 0.15 | 44.40 | ||
Sample nr. | Four Oceans | Cu2+ [µg/l] | Al3+ [µg/l] | Zn2+ [µg/l] | Cd2+ [µg/l] | Co2+ [µg/l] | Cr3+ [µg/l] | Mo4+ [µg/l] | Ni2+ [µg/l] | Pb2+ [µg/l] | SUM MICRO CATIONS |
Threshold | 0.10 | 0.30 | 0.30 | 0.01 | 0.01 | 0.02 | 0.18 | 0.03 | 0.04 | ||
1) | Netherlands | 0.13 | 0.30 | 0.30 | 0.01 | 0.01 | 0.01 | 2.07 | 0.03 | 0.04 | 2.90 |
2) | Indonesia | 0.02 | 0.70 | 0.30 | 0.00 | 0.01 | 0.01 | 1.14 | 0.36 | 0.04 | 2.58 |
3) | Cuba | 0.10 | 1.00 | 0.30 | 0.02 | 0.01 | 0.05 | 2.49 | 0.16 | 0.04 | 4.17 |
4) | Ireland | 0.10 | 0.30 | 0.30 | 0.00 | 0.01 | 0.00 | 1.11 | 0.03 | 0.04 | 1.89 |
Mean | 0.09 | 0.58 | 0.30 | 0.01 | 0.01 | 0.02 | 1.70 | 0.15 | 0.04 | 2.88 | |
Std | 0.05 | 0.34 | 0.00 | 0.01 | 0.00 | 0.02 | 0.69 | 0.16 | 0.00 | 0.95 | |
Sample | Ratio | Cu2+ [µg/l] | Al3+ [µg/l] | Zn2+ [µg/l] | Cd2+ [µg/l] | Co2+ [µg/l] | Cr3+ [µg/l] | Mo4+ [µg/l] | Ni2+ [µg/l] | Pb2+ [µg/l] | SUM MICRO CATIONS |
nr. | seaweed/ocean | ||||||||||
Threshold | 0.10 | 0.30 | 0.30 | 0.01 | 0.01 | 0.02 | 0.18 | 0.03 | 0.04 | ||
1) | Ulva/ocean | 2544.23 | 510.00 | 4107.50 | 199.17 | 1982.14 | 1865.00 | 6.92 | 5250.00 | 31.38 | 16496.34 |
571.49 | 69.97 | 789.95 | 28.57 | 47.20 | 90.37 | 0.49 | 322.61 | 41.40 | 1281.90 | ||
2) | Caulerpa sert./ocean | 3695.00 | 222.86 | 595.83 | 403.75 | 207.50 | 684.72 | 12.98 | 55.76 | 2.31 | 5880.72 |
639.07 | 14.19 | 61.49 | 65.24 | 23.69 | 29.74 | 2.63 | 10.81 | 3.84 | 826.12 | ||
3) | Caulerpa brach./ocean | 1.30 | 0.30 | 1.00 | 0.60 | 1.17 | 0.20 | 0.83 | 0.19 | 1.00 | 6.58 |
0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
4) | Undaria/ocean | 0.20 | 2.33 | 1.00 | 0.50 | 1.00 | 2.25 | 1.03 | 12.00 | 1.00 | 21.31 |
0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 |
Sample nr. | Seaweed Species | H+ Ions | pH | P3− [mg/l] | N-NH4 [mg/l] | (NO3 + NO2) [mg/l] | N-total [mg/l] | Sum nutrient (N & P) |
---|---|---|---|---|---|---|---|---|
Threshold | [mol/l] | X | 0.10 | 0.04 | 0.03 | 0.30 | ||
1) | Ulva lactuca | 0.64 | 5.06 | 0.00 | 0.00 | 0.01 | 0.20 | 0.21 |
0.17 | 0.17 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
2) | Caulerpa sertlaiodes | 1.66 | 4.19 | 0.02 | 0.02 | 0.86 | 1.00 | 1.90 |
0.02 | 0.02 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
3) | Caulerpa cf. Brach. | 2.65 | 4.51 | 0.79 | 0.02 | 14.10 | 14.70 | 29.61 |
0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
4) | Undaria pinnatifidia | 4.12 | 6.51 | 0.01 | 0.04 | 0.01 | 0.20 | 0.26 |
0.07 | 0.05 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
Sample nr. | Four Oceans | H+ Ions | pH | P3− [mg/l] | N-NH4 [mg/l] | (NO3 + NO2) [mg/l] | N-total [mg/l] | Sum nutrient (N & P) |
Threshold | [mol/l] | X | 0.10 | 0.04 | 0.03 | 0.30 | ||
1) | Netherlands | 0.25 | 8.29 | 0.02 | 0.04 | 0.03 | 0.20 | 0.29 |
2) | Indonesia | 0.25 | 8.12 | 0.02 | 0.02 | 0.86 | 1.00 | 1.90 |
3) | Cuba | 0.25 | 8.11 | 0.79 | 0.02 | 14.10 | 14.70 | 29.61 |
4) | Ireland | 0.25 | 7.96 | 0.01 | 0.04 | 0.01 | 0.20 | 0.26 |
Mean | 0.25 | 8.12 | 0.21 | 0.03 | 3.75 | 4.03 | 8.02 | |
Std | 0.13 | 0.13 | 0.39 | 0.01 | 6.91 | 7.13 | 14.42 | |
Sample nr. | Ratio seaweed/ocean | H+ Ions | pH | P3− [mg/l] | N-NH4 [mg/l] | (NO3 + NO2) [mg/l] | N-total [mg/l] | Sum nutrient (N & P) |
Threshold | [mol/l] | X | 0.10 | 0.04 | 0.03 | 0.30 | ||
1) | Ulva/ocean | 7.32 | 0.61 | 0.05 | 0.03 | 0.33 | 1.00 | 1.41 |
0.02 | 0.02 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
2) | Caulerpa sert./ocean | 2.25 | 0.80 | 0.50 | 2.00 | 0.01 | 0.20 | 2.71 |
0.01 | 0.01 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
3) | Caulerpa brach./ocean | 1.34 | 1.02 | 0.03 | 2.00 | 0.00 | 0.01 | 2.04 |
0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | ||
4) | Undaria/ocean | 1.35 | 1.02 | 2.00 | 0.50 | 86.00 | 5.00 | 93.50 |
0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 |
to maintain suitable ion levels by minimizing the influx of Na+ ions into cells via Na+-ATPase activity. In principle there are three major mechanisms a seaweed can apply in order to cope with the problem of salt stress in the euhaline oceanic environment [
First, Na+ sequesters in vacuoles within the lumen of the seaweed thallus in such a safe way that this salt is spatially separated from vital plant physiological and biochemical mechanisms. A cell-to-cell channel e.g. in case of the Na+ sequestering in special vacuoles within the lumen of the seaweed thallus with vacuoles for Na+ storage spatially separated from vital seaweed organelles like the nucleus, chloroplast with its essential enzymes for photosynthesis and mitochondria for vital plant physiological and biochemical mechanisms. While some seaweeds appear to minimize the influx of ions into cells, ion sequestering within vacuoles is still essential in maintaining osmotic equilibrium, in support of Na+ accumulation in vacuoles. In these plants, ATPases mediate the translocation of H+ and K+/Na+, and were found to increase in number during salt stress [
The [Wet weight/Dry weight] ratio WW/DW is a morphological parameter to make a comparison between seaweeds species possible to estimate the vacuole capacity and thus the water storage capacity. By using this mechanical pressure method until 10 bar we have to consider, we obtained seaweed moisture from two types of vacuoles: first, vacuoles from the epidermal cells with proportionally smaller vacuoles and secondly from the highly vacuolated mesophyll cells [
Secondly, active or passive extrusion of Na+ to the oceanic environment followed by finding solutions by absorption (passive or active) of several compounds Heavy Metals [HM] and nutrients like N & P or the ion K+ from the oceanic environment which can act as osmolyticum so that ionic homeostasis is maintained. Even with the disparity between Na+ and K+ concentrations in seawater at all four oceanic locations of ≈ 30 with of course [K+] ≈ 30 fold lower) our seaweeds are able to accumulate comparatively high levels of K+ within their tissues which correspond to the values for seagrasses (
Third, production by several specific adapted seaweed species of economical important osmolyticum after sodium extrusion is a rather metabolically and energetically expensive method which also from a biochemical point of view much has evolved during course of evolution in some specific seaweed species. It is a much “cheaper” way simply to exchange the extruded sodium ions with an osmolyticum which is already available in the oceanic environment like Heavy Metals and nutrients like N & P. However, during course of evolution some seaweed species “has chosen” for this option, which is nowadays in gratitude explored by industry because these osmolyticum compounds have many purposes and of extremely economic importance. Osmolytica like alginates and carrageenan are mainly produced by brown seaweeds while agar is mainly produced by red seaweeds. From the carbohydrate fraction these alginates are important cell wall component in all brown seaweed spp. constituting up to 40% - 47% of the dry weight of seaweed biomass. The alginates and their oxidation products the sugar-diacides are employed by seaweeds as a sequestering mechanism for heavy metals [HM] in the seaweed moisture. From the phycocoloid fraction carrageenans are a group of biomolecules composed of linear polysaccharide chains with sulphate half-esters attached to the sugar unit. These properties allow carrageenans to dissolve in water, form highly viscous solutions and remain stable over a wide pH range. Especially the brown seaweeds Chondrus crispus and Kappaphycus spp. can contain up to 71% and 88% of carrageenan, respectively. The other osmolyticum from the phycocoloid fraction -but in contrast to carrageenans extracted from red seaweed such as Gelidium spp. and Gracilaria spp. is agar. Agar is a mixture of polysaccharides, which can be composed of agarose and agropectin, with similar structural and functional properties as carrageenans. The agar content in Gracilaria spp. can reach values up to 31% [
Salt extrusion to the oceanic environment in exchange with a certain compound like metallic cations (Heavy metals [HM]) which serve as kind of osmolyticum to maintain cell integrity [
A third adaptation mechanism in some specific seaweeds (mainly red & brown) to salt extrusion is the production of its own osmolyticum. The several produced osmolytical compounds are in an extensive detailed manner mentioned by [
The permeability of biological membranes is highly selective. The flow of molecules and ions between a cell and its environment is regulated by specific transport systems which will be exemplified under A: Active and B: Passive. These transport systems have several important roles: 1) They regulate cell volume and maintain the intracellular pH and ionic composition within a narrow range to provide a favorable environment for enzyme activity; 2) The molecular mechanism of many transport processes is a very actual research area. With respect to seaweeds and other marine plants it is a nearly unexplored research area [
A: Active Of all transport mechanisms over the cell membrane the ATP driven Na+/K+ is the best described. For seaweeds in high saline environments it is believed that Na+ can cross the plasma membrane using the same transport systems developed for K+ [
This pump has two purposes:
B: Passive Many transport processes are not directly driven by the hydrolysis of ATP. Instead, they are coupled to the flow of an anion down its electrochemical gradient. An example is facilitated diffusion without any ATP costs. Overall, theoretically several mechanisms for transport of ions over cell membranes are possible. These are transporters (or carrier) proteins which can move a single type of molecule in one direction across the cell membrane (a uniporter), several different molecules in one direction (a symporter) or different molecules in opposite directions (an antiporter) [
This probably can be ascribed to proton transport across the plasma membrane and tonoplast driven by electrochemical gradients produced thus ATP-driven by H+ pumps ratio: [H+ seaweed]/[H+ ocean] [
From all four investigated seaweeds Ulva lactuca has probably the highest tolerance for salt stress. From the study of [
On one hand we have seaweed species (genetic) influences which we will elucidate in future studies by determination of species specific characteristics in the biochemical composition of the seaweed cell wall. The involved cell wall constituents for the three different seaweed Phyla (green, brown, red) are mentioned below.
1) For green seaweeds (three of our investigated species) the cell wall contains sulphuric acid polysaccharides, sulphated galactans and xylans,
2) For brown seaweeds like in this study Undaria pinnatifidia the cell wall consists of compounds like alginic acid, fucoidan (sulphated fucose), laminarin (β-1,3 glucan) and sargassan,
3) For red seaweeds the cell wall contains agars, carrageenans, xylans, floridean starch (amylopectin-like glucan), water-soluble sulphated galactan.
The cell walls of all these thousands of seaweeds are species-specific. So in our investigation of the topic of salt extrusion of the four selected seaweeds some of the different observation possibly can be explained by seaweed species characteristics. Just like we earlier published that for seaweed lipid compositions (the several Ω-3 and Ω-6 poly-unsaturated acids (PUFA’s), as well as its Ω-6/Ω-3 ration), both quantitatively as qualitatively were to a major extent seaweed species (genus) dependent, to a minor extent also an environmental effect [
Perspectives: While terrestrial agriculture is presently at its limits [
van Ginneken, V. (2018) Some Mechanism Seaweeds Employ to Cope with Salinity Stress in the Harsh Euhaline Oceanic Environment. American Journal of Plant Sciences, 9, 1191-1211. https://doi.org/10.4236/ajps.2018.96089