A New Niche for Anoxygenic Phototrophs as Endoliths

Abstract

Anoxygenic phototrophic bacteria (APBs) occur in a wide range of aquatic habitats, from hot springs to freshwater lakes and intertidal microbial mats. Here, we report the discovery of a novel niche for APBs: endoliths within marine littoral carbonates. In a study of 40 locations around Isla de Mona, Puerto Rico, and Menorca, Spain, 16S rRNA high-throughput sequencing of endolithic community DNA revealed the presence of abundant phylotypes potentially belonging to well-known APB clades. An phylogenetic classification of these sequences enabled us to refine the assignments more stringently. Even then, all locations contained such putative APBs, often reaching a significant proportion of all phototrophic sequences. In fact, in some 20% of samples, their contribution exceeded that of oxygenic phototrophs, previously regarded as the major type of endolithic microbe in carbonates. The communities contained representatives of APBs in the, various proteobacterial groups, and The most abundant phylotypes varied with geography: on Isla de Mona, and -related phylotypes dominated, whereas those related to were the most common in Menorca. The presence of active populations of APBs was corroborated through an analysis of photopigments: bacteriochlorophylls were detected in all samples, bacteriochlorophyll and being most abundant. We discuss the potential metabolism and geomicrobial roles of endolithic APBs. Phylogenetic inference suggests that APBs may be playing a role as photoheterotrophs, adding biogeochemical complexity to our understanding of such communities. Given the global extent of coastal carbonate platforms, they likely represent a very large and unexplored habitat for APBs. Endolithic microbial communities from carbonates, which have been explored for over 2 centuries in predominantly naturalistic studies, were thought to be primarily composed of eukaryotic algae and cyanobacteria. Our report represents a paradigm shift in this regard, at least for the marine environment, demonstrating the presence of ubiquitous and abundant populations of APBs in this habitat. It raises questions about the role of these organisms in the geological dynamics of coastal carbonates, including coral reefs.

Down to the bone: the role of overlooked endolithic microbiomes in reef coral health

“…Cyanobacteria were long thought to be the key players mediating nitrogen fixation in endolithic microbial communities, because of their abundance in coral skeletons and the previous report of nitrogen fixation by unicellular cyanobacteria within the tissue of Montastraea cavernosa [63]. However, recent studies have also identified the presence of ubiquitous populations of green sulfur bacteria, capable of anoxygenic photosynthesis and nitrogen fixation, in the coral skeleton [30,64]. These green sulfur bacteria harbour genes involved in nitrogen metabolism, including glutamine/glutamate synthases, reduction of hydroxylamine, and nitrogen fixation [47].…”

Succession and Colonization Dynamics of Endolithic Phototrophs within Intertidal Carbonates

“…As expected, phototroph colonization followed a similar trend with photopigment content increasing at a rate of 2.3 mg m −2 month −1 , reaching an average value of 7.22 mg m −2 by 9 months. (Figure 3b), at which point 16S rRNA gene counts were not significantly different from those found in steady-state climax communities described by Couradeau et al [14] and Roush et al [15] (Student's t-test, p < 0.05). While total chlorophyll pigment concentrations were not significantly different between 9 months and steady-state climax communities either, cyanobacteria-specific counts were actually higher at 9 months than in steady-state climax communities.…”

“…Three natural substrate samples from Couradeau et al [14] and Roush et al [15] (samples denoted as H001-H003 in SRA) were used as proxies for steady-state climax communities for comparison of colonization progress. The samples were chosen based upon their geographic proximity to the tile placement location and their similar geological composition (calcite).…”

“…Although early research was informative in identifying and characterizing major euendolithic players, the use of morphological characterization alone has been found to underestimate microbial diversity in endolithic cyanobacterial communities [12,13]. Indeed, in the case of marine carbonate communities, high-throughput amplicon sequencing has demonstrated that morphology-based studies can underrepresent cyanobacterial diversity estimates by factors of 10 to 100 [12,14,15]. Early research identified three major morphotypical groups of euendolithic cyanobacteria.…”

“…The most dominant APBs were members of the Chloroflexales (green nonsulfur bacteria) [21][22][23] and Erythrobacter (aerobic anoxygenic phototrophs) [24,25]. APBs could comprise upwards of 80% of the total phototroph community [15] in some samples. Our findings broadened the known habitats for APBs and suggested that some microscopic characterizations of endolithic thin filamentous organisms (Plectonema-like) may have in fact been APBs.…”