Structural and functional analysis of a microbial mat ecosystem from a unique permanent hypersaline inland lake: ‘La Salada de Chiprana’ (NE Spain)

Abstract

The benthic microbial mat community of the only permanent hypersaline natural inland lake of Western Europe, 'La Salada de Chiprana', northeastern Spain, was structurally and functionally analyzed. The ionic composition of the lake water is characterized by high concentrations of magnesium and sulfate, which were respectively 0.35 and 0.5 M at the time of sampling while the total salinity was 78 g l(-1). Community composition was analyzed by microscopy, high-performance liquid chromatography (HPLC) pigment analyses and by studying culturable bacteria from different functional groups. Therefore, denaturing gradient gel electrophoresis (DGGE) was applied on most probable number (MPN) dilution cultures. Microscopy revealed that a thin layer of Chloroflexus-like bacteria overlaid various cyanobacteria-dominated layers each characterized by different morphotypes. DGGE analysis of MPN dilution cultures from distinct mat layers showed that various phylotypes of anoxygenic phototrophic, aerobic heterotrophic, colorless sulfur-, and sulfate-reducing bacteria were present. The mats were furthermore functionally studied and attention was focussed on the relationship between oxygenic primary production and the flow of carbon through the microbial community. Microsensor techniques, porewater and sediment photopigment analysis were applied in order to estimate oxygenic photosynthetic rates, daily dynamics of (in)organic carbon porewater concentration and migration behavior of phototrophs. Chiprana microbial mats produced dissolved organic carbon (DOC) both during the day and night. It was estimated that 14% of the mats gross photosynthetic production and 49% of the mats net photosynthetic production diffused out of the mat in the form of low molecular mass fatty acids, although these compounds made up only 2% of the total DOC pool. The high flux of dissolved fatty acids from the microbial mat to the water column may explain why in this system Chloroflexus-like bacteria proliferate on top of the cyanobacterial layers since these photoheterotrophic bacteria grow preferably on organic phototrophic exudates. Furthermore it may also explain why high numbers of viable sulfate-reducing bacteria were found in the fully oxygenated sediment surface layers. These organisms apparently do not have to compete with aerobic heterotrophic community members due to the ample availability of organic substrates. Moreover, the high production of DOC strongly indicates that the mat community was nutrient limited in its growth. Photopigment analysis revealed furthermore that chlorophyll a (Chla) and three of its allomeres had a complementary depth distribution what suggests that the Chla allomeres are functional adaptations to differences in light quality and/or quantity and may be species specific.

Irradiance Regulation of Photosynthesis and Respiration in Modern Marine Microbialites Built by Benthic Cyanobacteria in a Tropical Lagoon (New Caledonia)

“…In contrast to the microbialite Phormidium sp TK1, these microbial mats are characterized by high respiration rates (Table 2). In these highly productive systems, heterotrophic bacteria are stimulated by the excretion of low molecular weight compounds, such as glycolate, lactate, or propionate, excreted by the photosynthetic microorganisms [26,27]. This tight coupling between heterotrophic respiration and oxygenic photosynthesis is not observed in the Phormidium sp TK1 microbialite, a finding that could be explained by different hypotheses.…”

“…Modern microbialites, including stromatolites, which that are usually called ''microbial mats,'' have been reported in very diverse environments, from freshwater [35] to hypersaline systems [23], and can thrive under a wide range of different temperatures, from polar regions to very hot deserts. While in temperate climates, large living microbial mats and microbialites are mostly restricted to so-called extreme environments where grazing pressure is reduced [27], in brackish and marine tropical environments these microbial structures are probably more widespread. Indeed, microbial mats cover large surface areas in Polynesian brackish ponds [37], and microbialites built by cyanobacteria are common in tropical lagoons such as those described for French Polynesia [45] and in New Caledonia (Camoin and Golubic, unpublished results).…”

Detection and Capturing of 14C Radioactively-Labeled Small Subunit rRNA from Mixed Microbial Communities of a Microbial Mat Using Magnetic Beads

“…Therefore, the failure to detect the RNA of Archaea and eukaryotes in our mats indicates that they are either very low in abundance or they are not playing a role in the carbon cycling in these mats. Diatoms were indeed observed by direct microscopy in these mats but at a much lower abundance than cyanobacteria [17]. The low detectability of archaeal and eukaryotic RNA could also be due to the low efficiency of hybridization.…”

“…The captured bacterial RNA, after washing out of the beads by heating, was still found to be labeled with 14 C. This labeled RNA belongs most likely to prokaryotic phototrophic microorganisms that fixed 14 C through the process of photosynthesis and possibly to heterotrophic bacteria that could have fed on radioactively labeled exudates. These phototrophs could include, in addition to cyanobacteria, chloroflexi as well as sulfur-oxidizing bacteria, which were shown abundant in these mats [17]. At this stage, it is not possible to identify exactly which bacteria have incorporated the label as the probe captures all bacterial rRNA, regardless of the presence or absence of the label.…”

“…Mat samples originated from a permanent hypersaline inland lake of Western Europe, 'La Salada de Chiprana', northeastern Spain were used in this study [17]. Mat cores (six cores, each 1 cm in diameter) were embedded in 5 ml 1.5% agarose in 6 separate glass tubes (Fig.…”