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Photosynthetic Pigments Contained in Surface Sediments from the Hydrothermal System of Guaymas Basin, Gulf of California

Photosynthetic Pigments Contained in Surface Sediments from the Hydrothermal System of Guaymas... Hindawi Journal of Marine Biology Volume 2019, Article ID 7484983, 8 pages https://doi.org/10.1155/2019/7484983 Research Article Photosynthetic Pigments Contained in Surface Sediments from the Hydrothermal System of Guaymas Basin, Gulf of California 1 2 3 D. B. Ram-rez-Ortega, L. A. Soto , A. Estradas-Romero , and F.E.Hernández-Sandoval ´ ´ UNAM, Circuito, Ciudad Universitaria, Coyoacan, 04510 Ciudad de Mexico, Mexico Instituto de Ciencias del Mar y Limnolog´ıa,UNAM,Circuito,Ciudad Universitaria,Coyoacan, ´ 04510 Ciudad de M´exico, Mexico Facultad de Ciencias. Circuito Exterior s/n, Coyoaca´n, Ciudad Universitaria, Coyoacan, ´ 04510 Ciudad de M´exico, Mexico Centro de Investigaciones Biologica ´ s del Noroeste, S.C. Km. 1 Carretera a San Juan de La Costa “EL COMITAN” Apdo. Postal 128, La Paz, BCS 23097, Mexico Correspondence should be addressed to L. A. Soto; lasg@cmarl.unam.mx Received 15 March 2019; Revised 6 May 2019; Accepted 23 May 2019; Published 1 July 2019 Academic Editor: Horst Felbeck Copyright © 2019 D. B. Ram´ırez-Ortega 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. ∘ 󸀠 ∘ 󸀠 ∘ 󸀠 In the exploration of the hydrothermal system of the Guaymas Basin (GB) between 27 00 35 and 27 00 50 N and 111 24 ∘ 󸀠 15 and 111 24 40 W in the Gulf of California, carried out on the R/V Atlantis and of the DSRV/Alvin in October 2008, four cores of surface sediments were obtained to analyse photosynthetic pigments at two locations with contrasting extreme conditions: Oil Town and Great Pagoda. We identified nine pigments: Chlorophyll-a ,Phaeophytin-a,Phaeophorbide-a, Pyropheophytin-a (degradation Chlorophyll-a products),𝛽 -Carotene, Alloxanthin, Zeaxanthin, Diadinoxanthin, and Prasinoxanthin (carotenoids). The maximum pigment concentration was registered in the Great Pagoda (10,309 ng/g) and the minimum in Oil Town (918 ng/g). It is demonstrated that photosynthetic pigment profiles in surface sediments depend on the heterogeneity of the extreme conditions of each site caused mainly by temperature and bacterial substrates. eTh refore, there were significant differences ( p<0.05) in the pigmentary profile of the four sedimentary cores analyzed. However, no statistical differences (p > 0.05) in the concentration of pigments have been detected. We conclude that the photosynthetic pigments contained in the surface sediments of the hydrothermal vents in the Guaymas Basin are primarily of chemoautotrophic bacterial origin. 1. Introduction in addition to the precipitates originated from hydrothermal u fl ids rich in particulate manganese and dissolved silica [4, 5]. An unusually high heat o fl w zone characterizes the Gulf Photosynthetic pigments contained in marine sediments of California due to convection currents in the magmatic are useful indicators of oxidized terrigenous organic matter chamber rising below this region through the Eastern Pacific and eutrophication conditions [6, 7] and have also been Rift (EPR) [1]. These propagation mechanisms of the crust in used in the evaluation of phototrophic communities [8]. the central Gulf of California, associated with intense tectonic Kowalewska [7] mentions that in a sedimentary sequence (0- dynamics of theplace,giveriseto a deep hydrothermal 10 cm), the content of pigments in the deep layers is similar system in the southern part of the Guaymas Basin (GB). The and generally lower than in the surface layers and that these sediments in Guaymas Basin are a mixture of immature, rfi st- dieff rences are caused by (1) sedimentation rates, (2) bacterial cycle erosional detritus, and biogenic material [1]. This system degradation, photooxidation, and temperature change in the is covered with a sedimentary layer rich in organic matter, water column, and (3) primary production. with a thickness of approximately 400 m [2]. It is composed The general biogeochemical conditions prevailing in GB of siliceous material of biogenic origin (mainly of diatoms are reasonably known [1, 9–13]. Our current knowledge > 50%) and terrigenous sediments rich in plagioclase [3], on the diagenesis of chlorophyll derivatives in the Gulf 󸀠󸀠 󸀠󸀠 󸀠󸀠 󸀠󸀠 2 Journal of Marine Biology 28 N 27 N 26 N ∘    11 26 W 24 22   04 ． 25 N 24 N 23 N ∘ ∘ 114 W 112 W ∘  27 00 Figure 1: Guaymas Basin (GB) and study area location in the Central Gulf of California. Modified from Soto [13]. of California is restricted to the geochemical analysis of hydrothermal landscape on the seao fl or [19], in which min- sediments obtained by the Deep Sea Drilling Project Leg 64 eral deposits are formed in the form of mounds, spires, [14]. Our study intends to elucidate if the composition and pagoda-like structures, and tall pillars distributed over a concentration of study’s focus is on the class of photosyn- terrain covered by fine sediment [9, 13] which contains a thetic pigments (tetrapyrrole and tetraterpenoid) contained complex mixture of aliphatic and aromatic hydrocarbons that in and their concentration in surface sediments from two are formed by the hydrothermal alteration of sedimentary active hydrothermal sites in GB suffered alteration due to organic matter [11, 18, 20]. the exhibiting contrasting extreme conditions prevailing at One of the sampling sites is the area called “Grand each site. We postulate that such conditions may alter the Pagoda.” It is a large hydrothermal formation. The area is diagenesis of chlorophyll derivatives as potential organic covered by orange and white Beggiatoa spp. bacterial mats sources for heterotrophs in the studied vent system. and Riftia colonies, indicating diffuse venting. In the upper part of the formation, it is covered by lobed extensions spreading that extend approximately one meter on each side 2. Materials and Methods towards the water column. Small chimneys appeared in the 2.1. Study Area. The Guaymas Basin is located in the central center of some flanges. Part of the hydrothermal u fl id flow ∘ 󸀠 ∘ part of the Gulf of California between 27 00 35 and 27 seeps and rises through the center of small chimneys [16]. The 󸀠 ∘ 󸀠 ∘ 󸀠 00 50 N and 111 24 15 and 111 24 40 W. It is a other site, “Old Town,” includes sulphide edifices with diffuse semienclosed Basin formed by two (northern and southern) flow, bearing clusters of R. pachyptila, but notorious for the axial troughs bounded by extensive systems of axial-parallel presence of liquid hydrocarbons in the adjacent sediments. fault lines separated by a fault 20 km long and 3 to 5 km The presence of organic carbon allows for high biological wide at a depth of 2,030 m with temperatures of 2.8 Cin the productivity at the site, despite being a zone of extreme condi- bottom [15–18] (Figure 1). The site is distinguished by having tions. The conjugation between sulphides and hydrocarbons a high sedimentation rate greater than 1-1.2 m 1,000 years- from hydrothermal discharges provides the necessary energy 1 [14] forming a combination of terrigenous detritus and for the development of a complex hydrothermal biological biogenic matter [1]. This high sedimentation rate favours the community whose existence depends on chemosynthetic concentration of considerable organic matter at the bottom of processes [13, 21]. the Basin that is subject to hydrothermal stress [9, 10, 14]. The most distinctive feature of the Basin is the active 2.2. Sampling. Four sediment push-cores (33 cm length x 16 hydrothermalism in the Southern Trough formed a complex cm diameter) were obtained during the AT 15-38 expedition 󸀠󸀠 󸀠󸀠 󸀠󸀠 󸀠󸀠 Journal of Marine Biology 3 0.9 0.8 0.7 Great Pagoda 0.6 0.5 Oil Town 0.4 3 10 ∘  27 0.3        ∘ 24.8 24.7 24.6 24.5 24.4 24.3 24.2 111 1cm:6.27 km Longitude (W) Figure 2: Spatial location of sediment cores recovered (3, 10, 1, and 11) by the DSRV-Alvin during the AT 15-38 campaign.∙ Active sites. on board of the R/V Atlantis in October 2010 at GB, Gulf 2.5. Statistical Analysis. AChi-square test (X )was per- of California (Figure 2). The push-cores were recovered by formed to determine whether the pigment type depended on the DSRV-2 Alvin (Woods Hole Oceanographic Institution) the sedimentary core from which the sample was extracted. during three dives at Oil Town and Great Pagoda located Similarly, an analysis of variance in a randomized block in the Southern Trough. Each site showed different physical design (ANDEVA) was applied to assess the existence of characteristics (Table 1). The sediment surface temperature significant statistical differences ( p≤ 0.05) in the concen- (0-30cm) was recordedwith the R/V Alvin High-TandLow- tration (ng/gr) and in the variety of pigments between the Tprobes. cores. Through Tukey’s multiple means comparison test ( p Once on board, the sediments of∼1cm fromthe seaofl or ≤0.05), the statistical differences between mean pigment were subsampled and stored under dark conditions at -70 C concentrations were determined [23]. until processed. Pigment analysis was performed according to the method described by Vidussi et al. [22] employing 3. Results high-performance liquid chromatography (HPLC). 3.1. Pigment Identicfi ation and Quanticfi ation. Nine pig- ments were identiefi d whose concentrations are listed in 2.3. Pigment Extraction. Five grams of surface sediment from Table 2. Six of these photosynthetic pigments corresponded to each core was processed. The extractions were made with 4 Chlorophyll-a,𝛽 -Carotene, Zeaxanthin, Alloxanthin, Diadi- cm of 100% HPLC grade acetone. The samples were kept in noxanthin, and Prasinoxanthin. The other three pigments, the dark for 24 h at -20 C. They were then centrifuged at 4,000 resulting from the Chl-a degradation, were Pyropheophytin- rpm for 15 min at 5 C. The extract was filtered through in 47 a,Phaeophytin-a,and Phaeophorbide-a (Figure 3). Not all mm fiberglass membrane and 0.45 𝜇 mpore size. The volume 3 ∘ the nine pigments identified were present in a single core. was recovered in 2 cm Eppendorf vials and stored at -20 C, In four cores, the most abundant Chl-a derivatives were 20𝜇 L; aer ft ward, the volume was injected into the High- Performance Liquid Chromatograph (Model 1100, Hewlett Pyropheophytin-a (3,684 ng/g), which represented 24.6% of Packard). the total concentration of pigments analyzed (14,962 ng/g), Phaeophorbide-a with 23.2% (3,478 ng/g), Phaeophytin-a 2.4. HPLC Pigment Analysis. A mobile phase was used by with 7.2% (1,074 ng/g), and Chlorophyll-a with 2.6% (386 mixing two solutions: Solution A: methanol HPLC grade ng/g) the least abundant. On the other hand, the pre- dominant carotenoid pigments were Prasinoxanthin (21.5%, combined with 1 N aqueous ammonium acetate to form a 70:30 v/v mixture and Solution B: methanol HPLC grade. The 3,209 ng/g),𝛽 -Carotene (14.1%, 2,114 ng/g), and Zeaxanthin separation was carried out in a Hypersil MOS C8 column 100 (5.6%, 841 ng/g). Diadinoxanthin and Alloxanthin had the lowest pigment concentration (168 and 8 ng/g, respectively) x 4.6 mm, 5𝜇 m particle size [22]. To identify the pigments, we compared the retention time of the sample peaks with (Table 2). those of the pure standards and the absorption spectra of the The highest pigment concentration was recorded in core problem sample with those of the generated library of the 11 (10,309 ng/g) and the lowest in core 3 (918 ng/g). Cores standards (precision< 1%). The pigments quantification was 1 and 10 had similar concentrations (1,876 and 1,859 ng/g, respectively). done by constructing a calibration curve (R =from 0.9107 to1) that include the concentrations for each standard (20, 30, 40, The presence of Phaeophorbide- a, Prasinoxanthin, Zeax- 50, 60, and 100 ng). anthin, and 𝛽 -Carotene was recorded in all the cores Latitude (N) 1cm:6.49 km 4 Journal of Marine Biology Table 1: Physical characteristics of the sediment samples obtained by the DSRV Alvin in the Guaymas Basin, Gulf of California (Cruise AT 15-38). DSRV-Alvin Immersion No. Core Location Position ∘ 󸀠 ∘󸀠 4457 3 Oil Town 27 00.7039 N 111 24.3179 W Substrate: the temperature recorded in the first 0-20 cm of depth was 30 C (ambient temperature). White and orange bacterial mats were found on surface. ∘ 󸀠 ∘ 󸀠 4459 10 Oil Town 27 00.7039 N 111 24.3179 W Substrate: the temperature recorded in the first 0-20 cm of depth was > 200 C. High concentrations of oil and gas were observed. The external matrix with bacterial growth, consisting of Beggiatoa spp. patches. ∘ 󸀠 ∘ 󸀠 4460 1 Great Pagoda 27 00.67636N11 24.416833 W Substrate: the temperature has a gradient of 19.2 to 71.0 C in the first 6 cm depth. Orange bacterial mat was found on surface. ∘ 󸀠 ∘ 󸀠 4460 11 Great Pagoda 27 00.67636N11 24.41683 W Substrate: the temperature has a gradient of 5 to 16 C in the first 6 cm depth. Olive green-black sediment. Yellow Beggiatoa spp. bacterial mat was found. Table 2: Retention time (min) and pigment concentration (ng/g) recorded in the sediment cores obtained at the Great Pagoda and Oil Town sites in the Guaymas Basin hydrothermal system. DL = detection limit (ng). A: absent. Pigment Profile Retention Time DL Each Pigment Concentration Great Pagoda Oil Town Tetraterpenoid 1 11 3 10 𝛽 -Carotene 14.7 0.14 440 914 341 419 Zeaxanthin 7.98 0.44 197 324 99 221 Alloxanthin 7.05 0.13 A A 8 A Diadinoxanthin 6.87 0.34 141 A 27 A Prasinoxanthin 6.03 0.22 820 1866 213 312 Tetrapyrrole Chlorophyll-a 12.39 0.23 A 298 A 87 Pyrophaeophytin-a 14.22 1.84 A 3514 169 A Phaeophytin-a 13.31 2.22 A 618 A 455 Phaeophorbide-a 5.02 1.36 277 2775 62 364 Pigments Concentration per Core 1876 10309 918 1859 Pigments Concentration Total 14,962 DAD1 A, Sig=440,1 Ref=off (UNAM\LUIS SOTO 2010.08.26 14-07-41\LUISSOTO 000005.D) mAU 0 2 4 6 8 10 12 14 16 18 min Figure 3: Chromatogram obtained from the sediment core 11. (1) Phaeophorbide-a , (2) Prasinoxanthin, (3) Diadinoxanthin, (4) Zeaxanthin, (5) Chlorophyll-a,(6) Phaeophytin-a, (7) Pyropheophytin-a,and (8)𝛽 -Carotene. Journal of Marine Biology 5 examined and only traces of Alloxanthin (8 ng/g) in core solar energy [29, 30]. The facultative photosynthetic bac- 11 (Table 2). Diadinoxanthin was present in cores 1 and teria (producers of bacteriochlorophyll or other pigments) 3, whereas Chl-a and Phaeophytin-a were only found in through a photochemical adaptation potential exploited at low levels of light take advantage of the photon flow emitted cores 10 and 11. The core 11 exhibited the maximum pigment concentration (10, 309 ng/g) in comparison with the other by hydrothermal u fl ids at extreme temperatures [30]. cores (Table 2), although in the core 3 there were also seven Chl-a is characterized by being less thermostable com- pigments identified in low concentrations. pared to Chl-b or c, depending on the environmental condi- With the Chi-square test (1% significance level), it is tions. The Chl- a molecule is highly susceptible, and therefore, concluded that the characteristics of the substrate and tem- its degradation is quite rapid [31, 32]. Approximately 90% perature of each recovered core with respect to the pigments of the Chl-a is broken down into colorless products [24]. concentration and presence registered in the study area are The degradation process is due to a combination of biotic factors (microorganisms or heterotrophic organisms) and independent (Chi-square test p <0.0001). In contrast, the estimated concentration for each identified pigment was abiotic factors (temperature, light intensity, and oxygen con- significantly different between the cores analyzed (ANDEVA, centration) that foster this process, whose final products are known as chloropigments, phaeopigments, or degradation F= 5.31, p> 0.006). However, no differences in the number of pigments recorded in each core were statistically significant products [24, 26, 33–36]. In the vent system of GB, the Chl-a (ANDEVA, F = 1.36, p = 0.26) degradation process due to the prevailing extreme conditions Tukey’s multiple comparison tests (p≤0.05) showed that resulted in the formation of Phaeophytin-a,Phaeophorbide- cores from Great Pagoda core 1 and Oil Town cores 3 and a, and Pyrophaeophytin-a. 10 did not have significant statistical differences since they The Phaeophytin- a is the product of the loss of magne- have a similar average pigment concentration. However, they sium in the Chl-a molecule [26, 34]. Afterward, its character- differed from core 11 from Great Pagoda which had the istic green color becomes an olive-brown tone. This pigment, like the Chl-a, was restricted to the cores 10 and 11, but highest average pigments concentration. with a higher relative concentrations (386 and 1074 ng/g, respectively). According to Yentsch [33], Chl-a fractions are 4. Discussions rapidly decomposed with the increase in water depth, the loss The study of pigments in marine sediments is relatively recent of light intensity, and the change in ambient temperature. When Chl-a loses a phytol group, Chlorophyllide is [6, 7]. Nevertheless, their analysis can provide vital informa- tion to determine the environmental conditions in a particu- formed, which in turn eliminates a magnesium molecule lar area. Chl-a represents the most common photosynthetic giving rise to Phaeophorbide-a [31, 35] showing that the Chl-a degradation to form Phaeophorbide-a is initiated by pigment in nature. It has been the focus of numerous studies because it is the best chemical indicator of phytoplankton extreme factors such as stress, light conditions, temperature biomass and sources of organic carbon [24]. It is also known changes, or their combined action. The presence of Chloro- phyllide in all the cores obtained in the study area is probably that Chl-a depends on light energy to maintain its activity and therefore, some inferences can be made concerning the light due to extreme physicochemical conditions promoted by the hydrothermal u fl ids liberated at venting sites of GB [1]; such and temperature conditions prevailing at the sites in which this photosynthetic pigment is detected [25]. Other pigments conditions seem to favor the formation of Phaeophorbide- are considered secondary or accessory since they represent a, which had the second highest concentration (3478 ng/g) among the nine pigments identified here. photoprotective cell membrane adaptations [26, 27]. Presumably, at depth in excess of 2,000 m, as is the The Pyrophaeophytin- a is the Chl-a degradation case of theGB, thelightconditions areoftotal darkness. final product which is formed by the decomposition of Phaeophytin-a, However, Reynolds and Lutz [28] have demonstrated that in due to the loss of a carboxyl group, thus the deep-ocean there are several sources of light, namely, bio- acquiring more stability and better preservation. Its presence luminescence, cosmic rays, and radioactivity. These authors indicates old and anoxic sediments with high organic carbon conclude that the spectral composition of this light is not content [7, 24, 26, 33]. visible for the human vision but can be detected by deep The high sedimentation rate of GB generates a thick layer of fine-grained sediments ( > 400 m) that favors the con- abyssal dwellers and perhaps contributes in maintaining the activity of photosynthetic pigments. This fact may explain centration of organic matter, reaching high organic carbon thepresenceofChl-a recorded in low concentrations in concentrations (3.4 to 12.4%) [2, 3, 10, 12]. Edgcomb et al. [37] mentioned that the Basin is a hydrothermally active cores 10 and 11 (298 and 87 ng/g, respectively, Table 2), occupying the third less abundant pigment (2.6%). Although environment that includes vent plugs, lfi trations, and anoxic these cores were spatially separated by approximately 20 sediments. These characteristics could explain the presence km, they were collected at substrate covered by extensive of Pyrophaeophytin-a (3,514 ng/g), Chl-a (298 ng/g), and bacterial mats and olive green sediments, indicative of Phaeophytin-a (618 ng/g) in the Great Pagoda core 11 and that thepossiblepresenceofChl-a or some of its derivatives of Pyrophaeophytin-a (169 ng/g) inthe Oil Towncore 3. (Phaeophytin-a,Phaeophorbide-a, or Pyrophaeophytin-a). In thepresentstudy, of theninepigmentsidentiefi d, It is worth mentioning that these findings add support to five belong to the group of carotenoids: 𝛽 -Carotene, Prasi- noxanthin, Zeaxanthin, Alloxanthin, and Diadinoxanthin. early assumptions that deep-sea hydrothermal ecosystems are capable of producing photosynthesis without relying on In theGulfofCalifornia, carotenoid downward ufl x is 6 Journal of Marine Biology attributed to the predominance of Bacillariophyceae [14]. On their structure. In GB, the𝛿 13 C signature of TOC surficial the other hand, Van Dover [30] pointed out that diverse sediments reveals depleted values (-32.0 ‰.) for sulfur-rich organisms that inhabit hydrothermal sites have the need sediments, while values are significantly enriched (-18.0‰) away from the vent, reflecting input of photosynthetic based to include carotenoid pigments in their diet, but they are unable to synthesize them. According to Neg ` re-Sadargues carbon [13]. et al. [38], carotenoid pigments are obtained from bacteria, fungi, or plants. DeBevoise et al. [39] suggested that the 5. Conclusions carotenoids found in the crab eggs of Bythograea thermydron Free-living organisms are essential in hydrothermal systems are produced in situ by chemoautotrophic bacteria present for the production of pigments. They function as sinks of and are not derived from phytodetritus as one may expect. inorganic sulphides and reducing components and promote 𝛽 -Carotene is found in almost all algae except Crypto- the production of organic carbon particles from inorganic phytes and Rhodophyta and is produced by a large number carbon, by complex bacterial consortiums, zooplankters, and of bacteria [36]. Its color is yellow, orange, or red and benthic organisms. The microorganisms inhabiting extreme is the most abundant carotenoid in nature [27]. Neg ` re- thermal and chemical environments have a high diversity Sadargues et al. [38] and DeBevoise et al. [39] identified this of metabolites and are essentially chemosynthetic. Although pigment as one of the factors responsible for the coloration cores 11 and 10 were obtained from different zones, Great of some crustaceans, such as Bythograea thermydron and Pagoda and Oil Town, respectively, they both shared sim- Rimicaris exoculata, both abundant in hydrothermal vent ilar Beggiatoa spp. substrate mats. The same occurred in sites of the Mid-Atlantic Ridge.𝛽 -Carotene was present in cores 1 and 3 from Great Pagoda and Oil Town, respec- all the sediment cores recovered at Great Pagoda and Oil tively, which presented large orange bacterial mats. Chl-a Town sites, where extensive bacterial mats of yellow, orange, and its derivatives (Phaeophytin-a,Phaeophorbide-a,and and red colors were detected. Diadinoxanthin has a yellow Pyrophaeophytin-a) attained their highest concentration in coloration which is probably formed by the conversion of core Great Pagoda 11, branded by its olive green color the final allylic group of neoxanthin, and Prasinoxanthin containing black large bacterial mats. The presence and is a dark pink pigment [36]. The main source of these concentration of the extracted pigments varied among sites. pigments is the exoskeleton or the tissues of some species of There were significant statistical differences in the concen- macrocrustaceans or molluscs [22]. The sampled sites in GB trations of pigments between cores. The nine photosynthetic probably involve a complex of chemoautotrophic bacterial pigments analyzed in this study seem to be a common feature consortiums capable of producing photosynthetic pigments in the surface sediments of the GB hydrothermal vent system [39–43]. whose presence and concentration under extreme thermal Alloxanthin and Zeaxanthin are orange or yellow pig- and chemical conditions essentially relies on the metabolism ments that belong to the group of xanthophylls and are of a diversity of the chemoautotrophic bacterial consortium. usually found in bacteria, algae, and higher plants or animals Guaymas Basin hydrothermal vents are rich in organic [36, 44]. Thepresenceof Alloxanthin inour study can again matter, sulphur, carbonates, and silicate materials. The pho- be ascribed to the existence of complex bacterial consortiums tosynthetic pigments accumulated in the surface sediments and to the occurrence of some copepods (e.g., Temora at venting sites of the GB hydrothermal system are essentially longicornis and Centropages hamatus) that concentrate this of chemoautotrophic bacterial origin. pigment in their digestive system [44]. On the other hand, Zeaxanthin can be an indicator of picocyanobacteria and cyanobacteria abundantly embedded in old sediments [45]. Data Availability Zeaxanthin does not have photoadaptive properties, so its The datasets generated during and/or analysed during the concentrationinacellcanbeconstantdespitechangesin light current study are available from the corresponding author conditions. Besides, it is so stable that it is considered a useful upon reasonable request. biomarker, even when the site conditions are oligotrophic including ancient sediments [45]. Another possible mechanism for the production of pig- Conflicts of Interest ments or degradation products occurs during the digestive The authors declare that there are no conflicts of interest process of some gastropods such as Littorina littorea [46] regarding the publication of this paper. which is distributed in the intertidal zone of the North Atlantic coasts.Thus,it cannot be ruled out that the pigments identified in the study area have a similar origin in bacteri- Acknowledgments ovorus molluscs associated with hydrothermal vents such as Provanna laevis [13]. Thanks are extended to H. Felbeck for his constructive The processes of vertical distribution of phaeopigments comments to this publication. This contribution was greatly in the ocean are not dismissed. Kalle [47] showed that sea- benefited by comments made by two anonymous reviewers. water contains soluble pigments produced by phytoplankton The authors express their gratitude to the members of the metabolism. However, studies conducted by other authors Harmful Microalgae Laboratory from Centro de Investiga- [26, 33, 48–51] did not reveal whether these pigments can ´ ciones Biologicas del Noroeste, S.C. (CIBNOR, S.C.) in La be accumulated at deep hydrothermal vents without altering Paz, Baja California Sur, for their assistance in the sample Journal of Marine Biology 7 processing.Thanks aredue to theWoods HoleOceano- [14] E. W. Baker and J. W. Louda, “Geochemistry of tetrapyrrole, tetraterpenoid, and perylene pigments in sediments from the graphic Institution for their invitation to participate in the Gulf of California: Deep Sea Drilling Project Leg 64, SITES 474, oceanographic cruise AT 15-38 on board of the R/V Atlantis. 477, 479, AND 481, and SCRIPPS Institution of Oceanography A special word of appreciation is due to the crew of the Guaymas Basin survey cruise LEG 3, sites 10G and 18G,” in ship and the DSRV Alvin for their invaluable support during Initial reports DSDP, Part 2,J.R. 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Photosynthetic Pigments Contained in Surface Sediments from the Hydrothermal System of Guaymas Basin, Gulf of California

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Hindawi Journal of Marine Biology Volume 2019, Article ID 7484983, 8 pages https://doi.org/10.1155/2019/7484983 Research Article Photosynthetic Pigments Contained in Surface Sediments from the Hydrothermal System of Guaymas Basin, Gulf of California 1 2 3 D. B. Ram-rez-Ortega, L. A. Soto , A. Estradas-Romero , and F.E.Hernández-Sandoval ´ ´ UNAM, Circuito, Ciudad Universitaria, Coyoacan, 04510 Ciudad de Mexico, Mexico Instituto de Ciencias del Mar y Limnolog´ıa,UNAM,Circuito,Ciudad Universitaria,Coyoacan, ´ 04510 Ciudad de M´exico, Mexico Facultad de Ciencias. Circuito Exterior s/n, Coyoaca´n, Ciudad Universitaria, Coyoacan, ´ 04510 Ciudad de M´exico, Mexico Centro de Investigaciones Biologica ´ s del Noroeste, S.C. Km. 1 Carretera a San Juan de La Costa “EL COMITAN” Apdo. Postal 128, La Paz, BCS 23097, Mexico Correspondence should be addressed to L. A. Soto; lasg@cmarl.unam.mx Received 15 March 2019; Revised 6 May 2019; Accepted 23 May 2019; Published 1 July 2019 Academic Editor: Horst Felbeck Copyright © 2019 D. B. Ram´ırez-Ortega 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. ∘ 󸀠 ∘ 󸀠 ∘ 󸀠 In the exploration of the hydrothermal system of the Guaymas Basin (GB) between 27 00 35 and 27 00 50 N and 111 24 ∘ 󸀠 15 and 111 24 40 W in the Gulf of California, carried out on the R/V Atlantis and of the DSRV/Alvin in October 2008, four cores of surface sediments were obtained to analyse photosynthetic pigments at two locations with contrasting extreme conditions: Oil Town and Great Pagoda. We identified nine pigments: Chlorophyll-a ,Phaeophytin-a,Phaeophorbide-a, Pyropheophytin-a (degradation Chlorophyll-a products),𝛽 -Carotene, Alloxanthin, Zeaxanthin, Diadinoxanthin, and Prasinoxanthin (carotenoids). The maximum pigment concentration was registered in the Great Pagoda (10,309 ng/g) and the minimum in Oil Town (918 ng/g). It is demonstrated that photosynthetic pigment profiles in surface sediments depend on the heterogeneity of the extreme conditions of each site caused mainly by temperature and bacterial substrates. eTh refore, there were significant differences ( p<0.05) in the pigmentary profile of the four sedimentary cores analyzed. However, no statistical differences (p > 0.05) in the concentration of pigments have been detected. We conclude that the photosynthetic pigments contained in the surface sediments of the hydrothermal vents in the Guaymas Basin are primarily of chemoautotrophic bacterial origin. 1. Introduction in addition to the precipitates originated from hydrothermal u fl ids rich in particulate manganese and dissolved silica [4, 5]. An unusually high heat o fl w zone characterizes the Gulf Photosynthetic pigments contained in marine sediments of California due to convection currents in the magmatic are useful indicators of oxidized terrigenous organic matter chamber rising below this region through the Eastern Pacific and eutrophication conditions [6, 7] and have also been Rift (EPR) [1]. These propagation mechanisms of the crust in used in the evaluation of phototrophic communities [8]. the central Gulf of California, associated with intense tectonic Kowalewska [7] mentions that in a sedimentary sequence (0- dynamics of theplace,giveriseto a deep hydrothermal 10 cm), the content of pigments in the deep layers is similar system in the southern part of the Guaymas Basin (GB). The and generally lower than in the surface layers and that these sediments in Guaymas Basin are a mixture of immature, rfi st- dieff rences are caused by (1) sedimentation rates, (2) bacterial cycle erosional detritus, and biogenic material [1]. This system degradation, photooxidation, and temperature change in the is covered with a sedimentary layer rich in organic matter, water column, and (3) primary production. with a thickness of approximately 400 m [2]. It is composed The general biogeochemical conditions prevailing in GB of siliceous material of biogenic origin (mainly of diatoms are reasonably known [1, 9–13]. Our current knowledge > 50%) and terrigenous sediments rich in plagioclase [3], on the diagenesis of chlorophyll derivatives in the Gulf 󸀠󸀠 󸀠󸀠 󸀠󸀠 󸀠󸀠 2 Journal of Marine Biology 28 N 27 N 26 N ∘    11 26 W 24 22   04 ． 25 N 24 N 23 N ∘ ∘ 114 W 112 W ∘  27 00 Figure 1: Guaymas Basin (GB) and study area location in the Central Gulf of California. Modified from Soto [13]. of California is restricted to the geochemical analysis of hydrothermal landscape on the seao fl or [19], in which min- sediments obtained by the Deep Sea Drilling Project Leg 64 eral deposits are formed in the form of mounds, spires, [14]. Our study intends to elucidate if the composition and pagoda-like structures, and tall pillars distributed over a concentration of study’s focus is on the class of photosyn- terrain covered by fine sediment [9, 13] which contains a thetic pigments (tetrapyrrole and tetraterpenoid) contained complex mixture of aliphatic and aromatic hydrocarbons that in and their concentration in surface sediments from two are formed by the hydrothermal alteration of sedimentary active hydrothermal sites in GB suffered alteration due to organic matter [11, 18, 20]. the exhibiting contrasting extreme conditions prevailing at One of the sampling sites is the area called “Grand each site. We postulate that such conditions may alter the Pagoda.” It is a large hydrothermal formation. The area is diagenesis of chlorophyll derivatives as potential organic covered by orange and white Beggiatoa spp. bacterial mats sources for heterotrophs in the studied vent system. and Riftia colonies, indicating diffuse venting. In the upper part of the formation, it is covered by lobed extensions spreading that extend approximately one meter on each side 2. Materials and Methods towards the water column. Small chimneys appeared in the 2.1. Study Area. The Guaymas Basin is located in the central center of some flanges. Part of the hydrothermal u fl id flow ∘ 󸀠 ∘ part of the Gulf of California between 27 00 35 and 27 seeps and rises through the center of small chimneys [16]. The 󸀠 ∘ 󸀠 ∘ 󸀠 00 50 N and 111 24 15 and 111 24 40 W. It is a other site, “Old Town,” includes sulphide edifices with diffuse semienclosed Basin formed by two (northern and southern) flow, bearing clusters of R. pachyptila, but notorious for the axial troughs bounded by extensive systems of axial-parallel presence of liquid hydrocarbons in the adjacent sediments. fault lines separated by a fault 20 km long and 3 to 5 km The presence of organic carbon allows for high biological wide at a depth of 2,030 m with temperatures of 2.8 Cin the productivity at the site, despite being a zone of extreme condi- bottom [15–18] (Figure 1). The site is distinguished by having tions. The conjugation between sulphides and hydrocarbons a high sedimentation rate greater than 1-1.2 m 1,000 years- from hydrothermal discharges provides the necessary energy 1 [14] forming a combination of terrigenous detritus and for the development of a complex hydrothermal biological biogenic matter [1]. This high sedimentation rate favours the community whose existence depends on chemosynthetic concentration of considerable organic matter at the bottom of processes [13, 21]. the Basin that is subject to hydrothermal stress [9, 10, 14]. The most distinctive feature of the Basin is the active 2.2. Sampling. Four sediment push-cores (33 cm length x 16 hydrothermalism in the Southern Trough formed a complex cm diameter) were obtained during the AT 15-38 expedition 󸀠󸀠 󸀠󸀠 󸀠󸀠 󸀠󸀠 Journal of Marine Biology 3 0.9 0.8 0.7 Great Pagoda 0.6 0.5 Oil Town 0.4 3 10 ∘  27 0.3        ∘ 24.8 24.7 24.6 24.5 24.4 24.3 24.2 111 1cm:6.27 km Longitude (W) Figure 2: Spatial location of sediment cores recovered (3, 10, 1, and 11) by the DSRV-Alvin during the AT 15-38 campaign.∙ Active sites. on board of the R/V Atlantis in October 2010 at GB, Gulf 2.5. Statistical Analysis. AChi-square test (X )was per- of California (Figure 2). The push-cores were recovered by formed to determine whether the pigment type depended on the DSRV-2 Alvin (Woods Hole Oceanographic Institution) the sedimentary core from which the sample was extracted. during three dives at Oil Town and Great Pagoda located Similarly, an analysis of variance in a randomized block in the Southern Trough. Each site showed different physical design (ANDEVA) was applied to assess the existence of characteristics (Table 1). The sediment surface temperature significant statistical differences ( p≤ 0.05) in the concen- (0-30cm) was recordedwith the R/V Alvin High-TandLow- tration (ng/gr) and in the variety of pigments between the Tprobes. cores. Through Tukey’s multiple means comparison test ( p Once on board, the sediments of∼1cm fromthe seaofl or ≤0.05), the statistical differences between mean pigment were subsampled and stored under dark conditions at -70 C concentrations were determined [23]. until processed. Pigment analysis was performed according to the method described by Vidussi et al. [22] employing 3. Results high-performance liquid chromatography (HPLC). 3.1. Pigment Identicfi ation and Quanticfi ation. Nine pig- ments were identiefi d whose concentrations are listed in 2.3. Pigment Extraction. Five grams of surface sediment from Table 2. Six of these photosynthetic pigments corresponded to each core was processed. The extractions were made with 4 Chlorophyll-a,𝛽 -Carotene, Zeaxanthin, Alloxanthin, Diadi- cm of 100% HPLC grade acetone. The samples were kept in noxanthin, and Prasinoxanthin. The other three pigments, the dark for 24 h at -20 C. They were then centrifuged at 4,000 resulting from the Chl-a degradation, were Pyropheophytin- rpm for 15 min at 5 C. The extract was filtered through in 47 a,Phaeophytin-a,and Phaeophorbide-a (Figure 3). Not all mm fiberglass membrane and 0.45 𝜇 mpore size. The volume 3 ∘ the nine pigments identified were present in a single core. was recovered in 2 cm Eppendorf vials and stored at -20 C, In four cores, the most abundant Chl-a derivatives were 20𝜇 L; aer ft ward, the volume was injected into the High- Performance Liquid Chromatograph (Model 1100, Hewlett Pyropheophytin-a (3,684 ng/g), which represented 24.6% of Packard). the total concentration of pigments analyzed (14,962 ng/g), Phaeophorbide-a with 23.2% (3,478 ng/g), Phaeophytin-a 2.4. HPLC Pigment Analysis. A mobile phase was used by with 7.2% (1,074 ng/g), and Chlorophyll-a with 2.6% (386 mixing two solutions: Solution A: methanol HPLC grade ng/g) the least abundant. On the other hand, the pre- dominant carotenoid pigments were Prasinoxanthin (21.5%, combined with 1 N aqueous ammonium acetate to form a 70:30 v/v mixture and Solution B: methanol HPLC grade. The 3,209 ng/g),𝛽 -Carotene (14.1%, 2,114 ng/g), and Zeaxanthin separation was carried out in a Hypersil MOS C8 column 100 (5.6%, 841 ng/g). Diadinoxanthin and Alloxanthin had the lowest pigment concentration (168 and 8 ng/g, respectively) x 4.6 mm, 5𝜇 m particle size [22]. To identify the pigments, we compared the retention time of the sample peaks with (Table 2). those of the pure standards and the absorption spectra of the The highest pigment concentration was recorded in core problem sample with those of the generated library of the 11 (10,309 ng/g) and the lowest in core 3 (918 ng/g). Cores standards (precision< 1%). The pigments quantification was 1 and 10 had similar concentrations (1,876 and 1,859 ng/g, respectively). done by constructing a calibration curve (R =from 0.9107 to1) that include the concentrations for each standard (20, 30, 40, The presence of Phaeophorbide- a, Prasinoxanthin, Zeax- 50, 60, and 100 ng). anthin, and 𝛽 -Carotene was recorded in all the cores Latitude (N) 1cm:6.49 km 4 Journal of Marine Biology Table 1: Physical characteristics of the sediment samples obtained by the DSRV Alvin in the Guaymas Basin, Gulf of California (Cruise AT 15-38). DSRV-Alvin Immersion No. Core Location Position ∘ 󸀠 ∘󸀠 4457 3 Oil Town 27 00.7039 N 111 24.3179 W Substrate: the temperature recorded in the first 0-20 cm of depth was 30 C (ambient temperature). White and orange bacterial mats were found on surface. ∘ 󸀠 ∘ 󸀠 4459 10 Oil Town 27 00.7039 N 111 24.3179 W Substrate: the temperature recorded in the first 0-20 cm of depth was > 200 C. High concentrations of oil and gas were observed. The external matrix with bacterial growth, consisting of Beggiatoa spp. patches. ∘ 󸀠 ∘ 󸀠 4460 1 Great Pagoda 27 00.67636N11 24.416833 W Substrate: the temperature has a gradient of 19.2 to 71.0 C in the first 6 cm depth. Orange bacterial mat was found on surface. ∘ 󸀠 ∘ 󸀠 4460 11 Great Pagoda 27 00.67636N11 24.41683 W Substrate: the temperature has a gradient of 5 to 16 C in the first 6 cm depth. Olive green-black sediment. Yellow Beggiatoa spp. bacterial mat was found. Table 2: Retention time (min) and pigment concentration (ng/g) recorded in the sediment cores obtained at the Great Pagoda and Oil Town sites in the Guaymas Basin hydrothermal system. DL = detection limit (ng). A: absent. Pigment Profile Retention Time DL Each Pigment Concentration Great Pagoda Oil Town Tetraterpenoid 1 11 3 10 𝛽 -Carotene 14.7 0.14 440 914 341 419 Zeaxanthin 7.98 0.44 197 324 99 221 Alloxanthin 7.05 0.13 A A 8 A Diadinoxanthin 6.87 0.34 141 A 27 A Prasinoxanthin 6.03 0.22 820 1866 213 312 Tetrapyrrole Chlorophyll-a 12.39 0.23 A 298 A 87 Pyrophaeophytin-a 14.22 1.84 A 3514 169 A Phaeophytin-a 13.31 2.22 A 618 A 455 Phaeophorbide-a 5.02 1.36 277 2775 62 364 Pigments Concentration per Core 1876 10309 918 1859 Pigments Concentration Total 14,962 DAD1 A, Sig=440,1 Ref=off (UNAM\LUIS SOTO 2010.08.26 14-07-41\LUISSOTO 000005.D) mAU 0 2 4 6 8 10 12 14 16 18 min Figure 3: Chromatogram obtained from the sediment core 11. (1) Phaeophorbide-a , (2) Prasinoxanthin, (3) Diadinoxanthin, (4) Zeaxanthin, (5) Chlorophyll-a,(6) Phaeophytin-a, (7) Pyropheophytin-a,and (8)𝛽 -Carotene. Journal of Marine Biology 5 examined and only traces of Alloxanthin (8 ng/g) in core solar energy [29, 30]. The facultative photosynthetic bac- 11 (Table 2). Diadinoxanthin was present in cores 1 and teria (producers of bacteriochlorophyll or other pigments) 3, whereas Chl-a and Phaeophytin-a were only found in through a photochemical adaptation potential exploited at low levels of light take advantage of the photon flow emitted cores 10 and 11. The core 11 exhibited the maximum pigment concentration (10, 309 ng/g) in comparison with the other by hydrothermal u fl ids at extreme temperatures [30]. cores (Table 2), although in the core 3 there were also seven Chl-a is characterized by being less thermostable com- pigments identified in low concentrations. pared to Chl-b or c, depending on the environmental condi- With the Chi-square test (1% significance level), it is tions. The Chl- a molecule is highly susceptible, and therefore, concluded that the characteristics of the substrate and tem- its degradation is quite rapid [31, 32]. Approximately 90% perature of each recovered core with respect to the pigments of the Chl-a is broken down into colorless products [24]. concentration and presence registered in the study area are The degradation process is due to a combination of biotic factors (microorganisms or heterotrophic organisms) and independent (Chi-square test p <0.0001). In contrast, the estimated concentration for each identified pigment was abiotic factors (temperature, light intensity, and oxygen con- significantly different between the cores analyzed (ANDEVA, centration) that foster this process, whose final products are known as chloropigments, phaeopigments, or degradation F= 5.31, p> 0.006). However, no differences in the number of pigments recorded in each core were statistically significant products [24, 26, 33–36]. In the vent system of GB, the Chl-a (ANDEVA, F = 1.36, p = 0.26) degradation process due to the prevailing extreme conditions Tukey’s multiple comparison tests (p≤0.05) showed that resulted in the formation of Phaeophytin-a,Phaeophorbide- cores from Great Pagoda core 1 and Oil Town cores 3 and a, and Pyrophaeophytin-a. 10 did not have significant statistical differences since they The Phaeophytin- a is the product of the loss of magne- have a similar average pigment concentration. However, they sium in the Chl-a molecule [26, 34]. Afterward, its character- differed from core 11 from Great Pagoda which had the istic green color becomes an olive-brown tone. This pigment, like the Chl-a, was restricted to the cores 10 and 11, but highest average pigments concentration. with a higher relative concentrations (386 and 1074 ng/g, respectively). According to Yentsch [33], Chl-a fractions are 4. Discussions rapidly decomposed with the increase in water depth, the loss The study of pigments in marine sediments is relatively recent of light intensity, and the change in ambient temperature. When Chl-a loses a phytol group, Chlorophyllide is [6, 7]. Nevertheless, their analysis can provide vital informa- tion to determine the environmental conditions in a particu- formed, which in turn eliminates a magnesium molecule lar area. Chl-a represents the most common photosynthetic giving rise to Phaeophorbide-a [31, 35] showing that the Chl-a degradation to form Phaeophorbide-a is initiated by pigment in nature. It has been the focus of numerous studies because it is the best chemical indicator of phytoplankton extreme factors such as stress, light conditions, temperature biomass and sources of organic carbon [24]. It is also known changes, or their combined action. The presence of Chloro- phyllide in all the cores obtained in the study area is probably that Chl-a depends on light energy to maintain its activity and therefore, some inferences can be made concerning the light due to extreme physicochemical conditions promoted by the hydrothermal u fl ids liberated at venting sites of GB [1]; such and temperature conditions prevailing at the sites in which this photosynthetic pigment is detected [25]. Other pigments conditions seem to favor the formation of Phaeophorbide- are considered secondary or accessory since they represent a, which had the second highest concentration (3478 ng/g) among the nine pigments identified here. photoprotective cell membrane adaptations [26, 27]. Presumably, at depth in excess of 2,000 m, as is the The Pyrophaeophytin- a is the Chl-a degradation case of theGB, thelightconditions areoftotal darkness. final product which is formed by the decomposition of Phaeophytin-a, However, Reynolds and Lutz [28] have demonstrated that in due to the loss of a carboxyl group, thus the deep-ocean there are several sources of light, namely, bio- acquiring more stability and better preservation. Its presence luminescence, cosmic rays, and radioactivity. These authors indicates old and anoxic sediments with high organic carbon conclude that the spectral composition of this light is not content [7, 24, 26, 33]. visible for the human vision but can be detected by deep The high sedimentation rate of GB generates a thick layer of fine-grained sediments ( > 400 m) that favors the con- abyssal dwellers and perhaps contributes in maintaining the activity of photosynthetic pigments. This fact may explain centration of organic matter, reaching high organic carbon thepresenceofChl-a recorded in low concentrations in concentrations (3.4 to 12.4%) [2, 3, 10, 12]. Edgcomb et al. [37] mentioned that the Basin is a hydrothermally active cores 10 and 11 (298 and 87 ng/g, respectively, Table 2), occupying the third less abundant pigment (2.6%). Although environment that includes vent plugs, lfi trations, and anoxic these cores were spatially separated by approximately 20 sediments. These characteristics could explain the presence km, they were collected at substrate covered by extensive of Pyrophaeophytin-a (3,514 ng/g), Chl-a (298 ng/g), and bacterial mats and olive green sediments, indicative of Phaeophytin-a (618 ng/g) in the Great Pagoda core 11 and that thepossiblepresenceofChl-a or some of its derivatives of Pyrophaeophytin-a (169 ng/g) inthe Oil Towncore 3. (Phaeophytin-a,Phaeophorbide-a, or Pyrophaeophytin-a). In thepresentstudy, of theninepigmentsidentiefi d, It is worth mentioning that these findings add support to five belong to the group of carotenoids: 𝛽 -Carotene, Prasi- noxanthin, Zeaxanthin, Alloxanthin, and Diadinoxanthin. early assumptions that deep-sea hydrothermal ecosystems are capable of producing photosynthesis without relying on In theGulfofCalifornia, carotenoid downward ufl x is 6 Journal of Marine Biology attributed to the predominance of Bacillariophyceae [14]. On their structure. In GB, the𝛿 13 C signature of TOC surficial the other hand, Van Dover [30] pointed out that diverse sediments reveals depleted values (-32.0 ‰.) for sulfur-rich organisms that inhabit hydrothermal sites have the need sediments, while values are significantly enriched (-18.0‰) away from the vent, reflecting input of photosynthetic based to include carotenoid pigments in their diet, but they are unable to synthesize them. According to Neg ` re-Sadargues carbon [13]. et al. [38], carotenoid pigments are obtained from bacteria, fungi, or plants. DeBevoise et al. [39] suggested that the 5. Conclusions carotenoids found in the crab eggs of Bythograea thermydron Free-living organisms are essential in hydrothermal systems are produced in situ by chemoautotrophic bacteria present for the production of pigments. They function as sinks of and are not derived from phytodetritus as one may expect. inorganic sulphides and reducing components and promote 𝛽 -Carotene is found in almost all algae except Crypto- the production of organic carbon particles from inorganic phytes and Rhodophyta and is produced by a large number carbon, by complex bacterial consortiums, zooplankters, and of bacteria [36]. Its color is yellow, orange, or red and benthic organisms. The microorganisms inhabiting extreme is the most abundant carotenoid in nature [27]. Neg ` re- thermal and chemical environments have a high diversity Sadargues et al. [38] and DeBevoise et al. [39] identified this of metabolites and are essentially chemosynthetic. Although pigment as one of the factors responsible for the coloration cores 11 and 10 were obtained from different zones, Great of some crustaceans, such as Bythograea thermydron and Pagoda and Oil Town, respectively, they both shared sim- Rimicaris exoculata, both abundant in hydrothermal vent ilar Beggiatoa spp. substrate mats. The same occurred in sites of the Mid-Atlantic Ridge.𝛽 -Carotene was present in cores 1 and 3 from Great Pagoda and Oil Town, respec- all the sediment cores recovered at Great Pagoda and Oil tively, which presented large orange bacterial mats. Chl-a Town sites, where extensive bacterial mats of yellow, orange, and its derivatives (Phaeophytin-a,Phaeophorbide-a,and and red colors were detected. Diadinoxanthin has a yellow Pyrophaeophytin-a) attained their highest concentration in coloration which is probably formed by the conversion of core Great Pagoda 11, branded by its olive green color the final allylic group of neoxanthin, and Prasinoxanthin containing black large bacterial mats. The presence and is a dark pink pigment [36]. The main source of these concentration of the extracted pigments varied among sites. pigments is the exoskeleton or the tissues of some species of There were significant statistical differences in the concen- macrocrustaceans or molluscs [22]. The sampled sites in GB trations of pigments between cores. The nine photosynthetic probably involve a complex of chemoautotrophic bacterial pigments analyzed in this study seem to be a common feature consortiums capable of producing photosynthetic pigments in the surface sediments of the GB hydrothermal vent system [39–43]. whose presence and concentration under extreme thermal Alloxanthin and Zeaxanthin are orange or yellow pig- and chemical conditions essentially relies on the metabolism ments that belong to the group of xanthophylls and are of a diversity of the chemoautotrophic bacterial consortium. usually found in bacteria, algae, and higher plants or animals Guaymas Basin hydrothermal vents are rich in organic [36, 44]. Thepresenceof Alloxanthin inour study can again matter, sulphur, carbonates, and silicate materials. The pho- be ascribed to the existence of complex bacterial consortiums tosynthetic pigments accumulated in the surface sediments and to the occurrence of some copepods (e.g., Temora at venting sites of the GB hydrothermal system are essentially longicornis and Centropages hamatus) that concentrate this of chemoautotrophic bacterial origin. pigment in their digestive system [44]. On the other hand, Zeaxanthin can be an indicator of picocyanobacteria and cyanobacteria abundantly embedded in old sediments [45]. Data Availability Zeaxanthin does not have photoadaptive properties, so its The datasets generated during and/or analysed during the concentrationinacellcanbeconstantdespitechangesin light current study are available from the corresponding author conditions. Besides, it is so stable that it is considered a useful upon reasonable request. biomarker, even when the site conditions are oligotrophic including ancient sediments [45]. Another possible mechanism for the production of pig- Conflicts of Interest ments or degradation products occurs during the digestive The authors declare that there are no conflicts of interest process of some gastropods such as Littorina littorea [46] regarding the publication of this paper. which is distributed in the intertidal zone of the North Atlantic coasts.Thus,it cannot be ruled out that the pigments identified in the study area have a similar origin in bacteri- Acknowledgments ovorus molluscs associated with hydrothermal vents such as Provanna laevis [13]. Thanks are extended to H. Felbeck for his constructive The processes of vertical distribution of phaeopigments comments to this publication. This contribution was greatly in the ocean are not dismissed. Kalle [47] showed that sea- benefited by comments made by two anonymous reviewers. water contains soluble pigments produced by phytoplankton The authors express their gratitude to the members of the metabolism. However, studies conducted by other authors Harmful Microalgae Laboratory from Centro de Investiga- [26, 33, 48–51] did not reveal whether these pigments can ´ ciones Biologicas del Noroeste, S.C. (CIBNOR, S.C.) in La be accumulated at deep hydrothermal vents without altering Paz, Baja California Sur, for their assistance in the sample Journal of Marine Biology 7 processing.Thanks aredue to theWoods HoleOceano- [14] E. W. Baker and J. W. Louda, “Geochemistry of tetrapyrrole, tetraterpenoid, and perylene pigments in sediments from the graphic Institution for their invitation to participate in the Gulf of California: Deep Sea Drilling Project Leg 64, SITES 474, oceanographic cruise AT 15-38 on board of the R/V Atlantis. 477, 479, AND 481, and SCRIPPS Institution of Oceanography A special word of appreciation is due to the crew of the Guaymas Basin survey cruise LEG 3, sites 10G and 18G,” in ship and the DSRV Alvin for their invaluable support during Initial reports DSDP, Part 2,J.R. 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