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  • Biogeosciences, 14, 959975, Author(s) 2017. CC Attribution 3.0 License.

    Biogeochemical cycling and phyto- and bacterioplanktoncommunities in a large and shallow tropical lagoon (TrminosLagoon, Mexico) under 20092010 El Nio Modokidrought conditionsPascal Conan1, Mireille Pujo-Pay1, Marina Agab1, Laura Calva-Bentez2, Sandrine Chifflet3, Pascal Douillet3,Claire Dussud1, Renaud Fichez3, Christian Grenz3, Francisco Gutierrez Mendieta2, Montserrat Origel-Moreno2,3,Arturo Rodrguez-Blanco1, Caroline Sauret1, Tatiana Severin1, Marc Tedetti3, Roco Torres Alvarado2, andJean-Franois Ghiglione11Sorbonne Universits, UPMC Univ Paris 06, CNRS, Laboratoire dOcanographie Microbienne (LOMIC),Observatoire Ocanologique, 66650, Banyuls/mer, France2Universidad Autnoma Metropolitana, Departamento de Hidrobiologa, Mxico D.F., Mexico3Aix-Marseille Universit, CNRSINSU, Universit de Toulon, IRD, Mediterranean Institute of Oceanography (MIO)UM 110, 13288, Marseille, France

    Correspondence to: Pascal Conan (

    Received: 8 July 2016 Discussion started: 11 August 2016Revised: 6 January 2017 Accepted: 25 January 2017 Published: 2 March 2017

    Abstract. The 20092010 period was marked by an episodeof intense drought known as the El Nio Modoki event. Sam-pling of the Trminos Lagoon (Mexico) was carried out inNovember 2009 in order to understand the influence of theseparticular environmental conditions on organic matter fluxeswithin the lagoons pelagic ecosystem and, more specifi-cally, on the relationship between phyto- and bacterioplank-ton communities. The measurements presented here concernbiogeochemical parameters (nutrients, dissolved and partic-ulate organic matter [POM], and dissolved polycyclic aro-matic hydrocarbons [PAHs]), phytoplankton (biomass andphotosynthesis), and bacteria (diversity and abundance, in-cluding PAH degradation bacteria and ectoenzymatic activ-ities). During the studied period, the water column of theTrminos Lagoon functioned globally as a sink and, moreprecisely, as a nitrogen assimilator. This was due to thehigh production of particulate and dissolved organic matter(DOM), even though exportation of autochthonous matter tothe Gulf of Mexico was weak. We found that bottom-upcontrol accounted for a large portion of the variability of phy-toplankton productivity. Nitrogen and phosphorus stoichiom-etry mostly accounted for the heterogeneity in phytoplank-ton and free-living prokaryote distribution in the lagoon. In

    the eastern part, we found a clear decoupling between ar-eas enriched in dissolved inorganic nitrogen near the PuertoReal coastal inlet and areas enriched in phosphate (PO4) nearthe Candelaria estuary. Such a decoupling limited the poten-tial for primary production, resulting in an accumulation ofdissolved organic carbon and nitrogen (DOC and DON, re-spectively) near the river mouths. In the western part of thelagoon, maximal phytoplankton development resulted frombacterial activity transforming particulate organic phospho-rus (PP) and dissolved organic phosphorus (DOP) to avail-able PO4 and the coupling between Palizada River inputs ofnitrate (NO3) and PP. The Chumpan River contributed onlymarginally to PO4 inputs due to its very low contribution tooverall river inputs. The highest dissolved total PAH concen-trations were measured in the El Carmen Inlet, suggestingthat the anthropogenic pollution of the zone is probably re-lated to the oil-platform exploitation activities in the shallowwaters of the southern of the Gulf of Mexico. We also foundthat a complex array of biogeochemical and phytoplanktonicparameters were the driving force behind the geographicaldistribution of bacterial community structure and activities.Finally, we showed that nutrients brought by the PalizadaRiver supported an abundant bacterial community of PAH

    Published by Copernicus Publications on behalf of the European Geosciences Union.

  • 960 P. Conan et al.: Trminos Lagoon, Mexico

    degraders, which are of significance in this important oil-production zone.

    1 Introduction

    Coastal lagoons are complex environments, combining fea-tures of shallow inland waterbodies wholly or partly sealedoff from the adjacent coastal oceans. They are influencedby tides, river inputs, the precipitation versus evaporationbalance, and the surface heat balance. Interactions betweenfreshwater and marine sources generate strong gradientsof salinity, light, and nutrient availability (Hauenstein andRamrez, 1986). Biological diversity is generally high inthese environments (Milessi et al., 2010). Located in thesouthern Gulf of Mexico near Campeche Sound, the Tr-minos Lagoon is one of the largest tropical coastal lagoonsworldwide, and its recognized environmental importance andprotected status are potentially threatened by petroleum-related industrial activities inshore and offshore (Garca-Roset al., 2013). A first tentative budget of salt and nutrients con-cluded that the Trminos Lagoon was slightly autotrophicon a yearly basis (David, 1999), but this assessment wasclearly based on scarce environmental data. Chlorophyll a(Chl a) concentration and phytoplankton net production havebeen reported to range from 1 to 17 g L1 and from 20 to300 gC m2 yr1 respectively (Day et al., 1982), suggestinga potential shift from oligotrophic to eutrophic conditions.

    In aquatic ecosystems, bacteria utilize a large fraction (upto 90 %) of the primary production, since algal carbon ex-udates can be the principal source for bacterial production(Cole et al., 1988; Conan et al., 1999). Besides the utiliza-tion of a considerable part of the available organic matter,bacterioplankton communities also absorb inorganic nutri-ents, thus competing with phytoplankton communities (Co-nan et al., 2007; Hobbie, 1988). The bulk of the organic mat-ter is a highly heterogeneous matrix which is primarily com-posed of complex and refractory substrates (Hoppe et al.,2002), but which also contains labile substrates such as pro-teins or peptides, oligosaccharides, and fatty acids. Extracel-lular enzymes are thus essential to aquatic microorganisms asthey allow for the partitioning of complex organic substrates,including high molecular weight compounds which cannotpass through the cell membrane (Arnosti and Steen, 2013).As a function of genetic diversity, the capacity to produce ex-tracellular enzymes is differently distributed in the bacterialcommunity, directly impacting the range of substrates me-tabolized (Zimmerman et al., 2013). This phenomenon hasglobal-scale implications since several meta-analyses haveclearly evidenced differences in the metabolic capacities ofmicroorganisms from temperate, tropical, or high latitudewaters (Amado et al., 2013; Arnosti et al., 2011). At a lo-cal scale, alteration of the evaporationprecipitation balancedue to climate change can be challenging, especially in the

    case of a coastal lagoon, as it is well known that changesin salinity may alter bacterial diversity and activity (Pedrs-Ali et al., 2000). Local anthropogenic inputs of organicpollutants such as polycyclic aromatic hydrocarbons (PAHs)may also affect bacterial diversity and activity (Aguayo et al.,2014; Jimnez et al., 2011; Rodrguez-Blanco et al., 2010).Indeed, PAHs, which can comprise as much as 2535 % oftotal hydrocarbon content in crude oils (Head et al., 2006),are among the most abundant and ubiquitous pollutants inthe coastal environment (Gonzlez-Gaya et al., 2016). Thesecompounds are recognized by the European and US environ-mental agencies as priority pollutants for the aquatic mediumdue to their toxicity, persistence, and ability to accumulate inthe biota (Kennish, 1992). Hence, the presence of PAHs inthe marine environment may induce an increase in the in-digenous populations of marine bacteria that can break downand utilize these chemicals as a carbon source, the so-calledPAH-degrading bacteria or PAH degraders. These bac-teria are generally strongly selected in oil-impacted ecosys-tems, where they may account for 70 to 90 % of the total bac-terial community (Gutierrez et al., 2014; Head et al., 2006).

    Despite their importance, few studies have consideredthe bacterial communities of tropical inland aquatic ecosys-tems (Roland et al., 2010) or coastal lagoons (Abreu et al.,1992; Hsieh et al., 2012; MacCord et al., 2013; They et al.,2013) and almost none have dealt with tropical coastal la-goons (Scofield et al., 2015). Among the existing studies,very few have been conducted on bacterial communities andmost of them have been based on culture-dependent meth-ods (Lizrraga-Partida et al., 1987, 1986). However, cul-tivable bacteria represent a very small fraction of the totalpresent bacteria (< 0.1 %; Ferguson et al., 1984), and culture-independent methods are needed to more accurately assessthe diversity and activity of whole bacterial communities insuch a vast and understudied system. Additionally, the Tr-minos Lagoon is potentially impacted by PAHs which maycome from a variety of sources which all carry various ur-ban and industrial wastes (fuel combustion and traffic ex-haust emissions) including sea-based activities (ballast wa-ter discharge, drilling, and spills from ships, platforms andpipelines), rivers, surface runoffs, and the atmosphere. Nev-ertheless, to our knowledge, little is known about the PAHcontent in this ecosystem. Even though Norea-Barroso etal. (1999) reported on PAH concentrations in the Ameri-can oyster Crassostrea virginica and Osten-Von Rendon etal. (2007) studied PAH concentrations in surface sediments,no data are currently available concerning dissolved PAHconcentrations in the surface waters of the Trminos Lagoon.

    Our study aims to evaluate the link between (i) biogeo-chemical (nutrients, dissolved and particulate organic matter[POM]), (ii) phytoplanktonic (biomass and photosyntheticactivity), and (iii) free-living prokaryote (diversity, includingPAH-degrading bacteria, and ectoenzymatic activities) pa-rameters in the water column of the Trminos Lagoon (Mex-ico) after a sustained period of minimum river discharge rel-

    Biogeosciences, 14, 959975, 2017

  • P. Conan et al.: Trminos Lagoon, Mexico 961

    Figure 1. Study site location and distribution of the 35 sampledstations in the lagoon.

    ative to the 20092010 El Nio Modoki episode. After hav-ing identified the main sources of nutrients in the lagoon (fo-cused on nitrogen and phosphorus), we propose a geograph-ical organization of the ecosystem to explain the distributionof the microbial pelagic communities across the lagoon.

    2 Materials and methods

    2.1 Study site and sampling

    The Trminos Lagoon is a large (1936 km2, volume4.65 km3) and shallow (average depth 2.4 m) coastal lagoonlocated in the Mexican state of Campeche (Fig. 1), 1820

    to 1900 N and 9110 to 9200W. Temperature showslow seasonal variation (27 to 33 C), but salinity oscillatesfrom brackish to marine waters due to high variability inriver runoffs (Fichez et al., 2016; Gullian-Klanian et al.,2008). River discharge, precipitation, and groundwater seep-age account for 95.44, 4.53 and 0.03 %, respectively. TheChumpan, CandelariaMamantel (hereafter Candelaria), andPalizada Estuaries account for 5, 19, and 76 %, respectively,of the freshwater delivered yearly ( 12 109 m3 yr1; i.e.about 2.6 times the lagoon volume) to the lagoon (Fichezet al., 2016). The lagoon is connected to the coastal sea bytwo inlets: El Carmen on the northwestern side (4 km long)and Puerto Real on the northeastern side (3.3 km in length).About half of the water volume is renewed every 9 days,mostly as a result of tidal exchange. The tide is mainly diur-nal, with a mean range of 0.3 m. (David and Kjerfve, 1998).Recent results on tidal current modeling (Contreras Ruiz Es-

    parza et al., 2014) reveal both a dynamic inshore currententering the lagoon through the El Carmen Inlet, flowingthrough the southern half of the lagoon and exiting throughPuerto Real, and a much slower inverse water current flood-ing the northern central part of the lagoon. This tidally in-duced hydrodynamic trend generates a counterclockwise cir-culation gyre located in the center of the lagoon, on the lee-ward side of Carmen Island.

    Samples were collected at a 0.2 m depth at 35 stationsdistributed over the whole lagoon (Fig. 1) from 21 to the27 October 2009. In 2009, a yearly cumulative discharge of4.83 1.71 109 m3 broke a historical deficit record overthe 19922011 period for the Palizada River (average yearlycumulative discharge of 7.19 4.22 109 m3 yr1) (Fichezet al., 2017). That exceptional drought period impacted theentire formerly Mesoamerican region during the 20092010El Nio Modoki episode. This resulted in a positive salin-ity anomaly in the Trminos Lagoon that developed moststrongly during the post-wet season period (Fichez et al.,2016) at the time of our sampling.

    A vertical profile of temperature, salinity, and fluorescencewas carried out at each of the 35 stations using a SeaBirdCTD probe (SBE 19) with a precision of 0.01 C for temper-ature and 0.001 for salinity. Once the profile was completed,water was sampled using a 5 L Niskin bottle maintained hor-izontally at 0.2 m below the surface.

    2.2 Nutrients and dissolved organic matter

    As soon as the Niskin sampler was retrieved on board, apreviously acid-washed 40 mL Schott

    glass vial was rinsed

    with sampled water, filled, immediately injected with the flu-orometric detection reagent for ammonia determination (asdescribed in Holmes et al., 1999), sealed, and stored in thedark for later analysis in the laboratory. Following this, two30 mL and one 150 mL plastic acid-washed vials were thenrinsed with sampled water, filled, and stored in a specificallydedicated and refrigerated ice cooler, to be later deep-frozenin the laboratory while awaiting analysis of dissolved inor-ganic and organic nutrients, as follows:

    Nitrate (NO3 0.02 M), nitrite (NO2 0.01 M), phos-phate (PO4 0.01 M), and silicate (Si(OH)4 0.05 M)concentrations were measured on a continuous flowTechnicon

    AutoAnalyzer II (Aminot and Krouel, 2007),

    as previously described in Severin et al. (2014). Ammonium(NH4 10 nM) was detected at nanomolar concentrations byfluorometric detection (Holmes et al., 1999) on a Turner De-signs Trilogy fluorometer.

    Samples for dissolved organic matter (DOM) were filteredthrough two precombusted (24 h, 450 C) glass fiber filters(Whatman GF/F, 25 mm). A total of 20 mL of dissolved or-ganic carbon (DOC) was collected in precombusted glasstubes, acidified with orthophosphoric acid (H3PO4), andanalyzed by high temperature catalytic oxidation (HTCO)(Cauwet, 1999) on a Shimadzu TOCV analyzer. Typical ana- Biogeosciences, 14, 959975, 2017

  • 962 P. Conan et al.: Trminos Lagoon, Mexico

    lytical precision is0.10.5 (SD) or 0.21 % (CV). A total of20 mL of dissolved organic nitrogen (DON) and phosphorus(DOP) was collected in Teflon vials and analyzed by Persul...