Chemosynthetic symbioses are partnerships between invertebrate animals and chemosynthetic bacteria. The latter are the primary producers, providing most of the organic carbon needed for the animal host's nutrition. We sequenced genomes of the chemosynthetic symbionts from the lucinid bivalve Loripes lucinalis and the stilbonematid nematode Laxus oneistus. The symbionts of both host species encoded nitrogen fixation genes. This is remarkable as no marine chemosynthetic symbiont was previously known to be capable of nitrogen fixation. We detected nitrogenase expression by the symbionts of lucinid clams at the transcriptomic and proteomic level. Mean stable nitrogen isotope values of Loripes lucinalis were within the range expected for fixed atmospheric nitrogen, further suggesting active nitrogen fixation by the symbionts. The ability to fix nitrogen may be widespread among chemosynthetic symbioses in oligotrophic habitats, where nitrogen availability often limits primary productivity.S ymbioses between animals and chemosynthetic bacteria are widespread in Earth's oceans 1 . Animals from at least seven phyla have formed such symbioses, and even more chemosynthetic bacterial lineages have evolved symbioses with animal hosts 1 . Chemosynthetic symbionts can use a range of chemicals, such as sulfide, methane, hydrogen and carbon monoxide, to power their metabolism 2-4 . The hosts of chemosynthetic symbionts dominate some animal communities. For example, shallow-water lucinid bivalves, which host sulfur-oxidizing symbionts, often dominate the macrobenthic infaunal community in seagrass meadows, where they can reach densities greater than 3,500 individuals per square metre 5,6 . Their diversity in nature, their persistence over evolutionary timescales and their dominance in many habitats attest to the success of these symbiotic partnerships 1 .Chemosynthetic symbionts are primarily considered 'nutritional symbionts', meaning their primary role is to provide nutrition for their hosts 1,7 . So far, most studies have focused on inorganic carbon fixation by the symbionts and the transfer of fixed organic carbon compounds to the hosts. In addition to organic carbon, all animals require a source of fixed nitrogen. However, nitrogen metabolism in chemosynthetic symbioses has received far less attention. Chemosynthetic symbionts have been shown to gain their nitrogen from ammonium or nitrate in their environment 8-10 and co-occurring nitrogen-fixing and chemosynthetic symbionts have been found in cold-water corals 11 . Nitrogen fixation by chemosynthetic symbionts has long been hypothesized, but so far not yet shown [12][13][14] .Our study focused mainly on the endosymbiosis between bivalves of the family Lucinidae and sulfur-oxidizing bacteria. Lucinids are by far the most diverse and widespread group of bivalves that host chemosynthetic symbionts 15 . There are at least 400 living species, occupying a range of habitats including mangrove sediments, seagrass beds, coral reef sediments and coastal mud and sand 16 . In seagrass...
Soda lakes are saline and alkaline ecosystems that are believed to have existed throughout the geological record of Earth. They are widely distributed across the globe, but are highly abundant in terrestrial biomes such as deserts and steppes and in geologically interesting regions such as the East African Rift valley. The unusual geochemistry of these lakes supports the growth of an impressive array of microorganisms that are of ecological and economic importance. Haloalkaliphilic Bacteria and Archaea belonging to all major trophic groups have been described from many soda lakes, including lakes with exceptionally high levels of heavy metals. Lonar Lake is a soda lake that is centered at an unusual meteorite impact structure in the Deccan basalts in India and its key physicochemical and microbiological characteristics are highlighted in this article. The occurrence of diverse functional groups of microbes, such as methanogens, methanotrophs, phototrophs, denitrifiers, sulfur oxidizers, sulfate reducers and syntrophs in soda lakes, suggests that these habitats harbor complex microbial food webs that (a) interconnect various biological cycles via redox coupling and (b) impact on the production and consumption of greenhouse gases. Soda lake microorganisms harbor several biotechnologically relevant enzymes and biomolecules (for example, cellulases, amylases, ectoine) and there is the need to augment bioprospecting efforts in soda lake environments with new integrated approaches. Importantly, some saline and alkaline lake ecosystems around the world need to be protected from anthropogenic pressures that threaten their long-term existence.
Sponges host a remarkable diversity of microbial symbionts, however, the benefit their microbes provide is rarely understood. Here, we describe two new sponge species from deep-sea asphalt seeps and show that they live in a nutritional symbiosis with methane-oxidizing (MOX) bacteria. Metagenomics and imaging analyses revealed unusually high amounts of MOX symbionts in hosts from a group previously assumed to have low microbial abundances. These symbionts belonged to the Marine Methylotrophic Group 2 clade. They are host-specific and likely vertically transmitted, based on their presence in sponge embryos and streamlined genomes, which lacked genes typical of related free-living MOX. Moreover, genes known to play a role in host–symbiont interactions, such as those that encode eukaryote-like proteins, were abundant and expressed. Methane assimilation by the symbionts was one of the most highly expressed metabolic pathways in the sponges. Molecular and stable carbon isotope patterns of lipids confirmed that methane-derived carbon was incorporated into the hosts. Our results revealed that two species of sponges, although distantly related, independently established highly specific, nutritional symbioses with two closely related methanotrophs. This convergence in symbiont acquisition underscores the strong selective advantage for these sponges in harboring MOX bacteria in the food-limited deep sea.
Cycloclasticus bacteria are ubiquitous in oil-rich regions of the ocean and are known for their ability to degrade polycyclic aromatic hydrocarbons (PAHs). In this study, we describe Cycloclasticus that have established a symbiosis with Bathymodiolus heckerae mussels and poecilosclerid sponges from asphalt-rich, deep-sea oil seeps at Campeche Knolls in the southern Gulf of Mexico. Genomic and transcriptomic analyses revealed that in contrast to all known Cycloclasticus, the symbiotic Cycloclasticus appeared to lack the genes needed for PAH degradation. Instead, these symbionts use propane and other short-chain alkanes such as ethane and butane as carbon and energy sources, thus expanding the limited range of substrates known to power chemosynthetic symbioses. Analyses of short-chain alkanes in the environment of the Campeche Knolls symbioses revealed that these are present at high concentrations (in the µM to mM range). Comparative genomic analyses revealed high similarities between the genes used by the symbiotic Cycloclasticus to degrade short-chain alkanes and those of free-living Cycloclasticus that bloomed during the Deepwater Horizon (DWH) oil spill. Our results indicate that the metabolic versatility of bacteria within the Cycloclasticus clade is higher than previously assumed, and highlight the expanded role of these keystone species in the degradation of marine hydrocarbons.
Lonar Lake is a unique saline and alkaline ecosystem formed by meteor impact in the Deccan basalts in India around 52 000 years ago. To investigate the role of methylotrophy in the cycling of carbon in this unusual environment, stable-isotope probing (SIP) was carried out using the onecarbon compounds methane, methanol and methylamine. Denaturing gradient gel electrophoresis fingerprinting analyses performed with heavy 13 C-labelled DNA retrieved from sediment microcosms confirmed the enrichment and labelling of active methylotrophic communities. Clone libraries were constructed using PCR primers targeting 16S rRNA genes and functional genes. Methylomicrobium, Methylophaga and Bacillus spp. were identified as the predominant active methylotrophs in methane, methanol and methylamine SIP microcosms, respectively. Absence of mauA gene amplification in the methylamine SIP heavy fraction also indicated that methylamine metabolism in Lonar Lake sediments may not be mediated by the methylamine dehydrogenase enzyme pathway. Many gene sequences retrieved in this study were not affiliated with extant methanotrophs or methylotrophs. These sequences may represent hitherto uncharacterized novel methylotrophs or heterotrophic organisms that may have been cross-feeding on methylotrophic metabolites or biomass. This study represents an essential first step towards understanding the relevance of methylotrophy in the soda lake sediments of an unusual impact crater structure.
SummaryIn the deep ocean, the conversion of methane into derived carbon and energy drives the establishment of diverse faunal communities. Yet specific biological mechanisms underlying the introduction of methane-derived carbon into the food web remain poorly described, due to a lack of cultured representative deep-sea methanotrophic prokaryotes. Here, we characterize the response of the deep-sea aerobic methanotroph Methyloprofundus sedimenti to methane starvation and recovery. By combining lipid analysis, RNA analysis, and electron cryotomography, we show that M. sedimenti undergoes discrete cellular shifts in response to methane starvation, including changes in headgroup-specific fatty acid saturation levels, and reductions in cytoplasmic storage granules. Methane starvation is associated with a significant increase in the abundance of gene transcripts pertinent to methane oxidation. Methane reintroduction to starved cells stimulates a rapid, transient extracellular accumulation of methanol, revealing a way in which methane-derived carbon may be routed to community members. This study provides new understanding of methanotrophic responses to methane starvation and recovery, and lays the initial groundwork to develop Methyloprofundus as a model chemosynthesizing bacterium from the deep sea.
Soda lakes constitute extreme aquatic ecosystems with remarkably high primary productivity rates, but information on the diversity and activity of methanogens in such environments is sparse. Using 16S rRNA and functional genes, we investigated the diversity of methanogens in the sediments of Lonar Lake, a unique saline and alkaline ecosystem formed by meteorite impact in the Deccan basalts. Although domain and phylum level 16S rRNA gene libraries were dominated by phylotypes related to Halobacteriales, sequences related to potentially novel Archaea within the orders Methanosarcinales and Methanomicrobiales were obtained together with a significant fraction of sequences representing uncultivated Euryarchaeota [Correction added after online publication 16 April 2012: orders 'Methanosarcina and Methanomicrobiaceae' changed to 'Methanosarcinales and Methanomicrobiales']. To identify the active methylotrophic Archaea involved in methanogenesis, mRNA transcripts of mcrA were retrieved from methanol consuming and methane emitting sediment microcosms at two different time points. Reverse-transcription PCR, qPCR, DGGE fingerprint, and clone library analysis showed that the active Archaea were closely related to Methanolobus oregonensis. To our knowledge, this is the first study identifying active methylotrophic methanogens in such an environment.
Methylophaga lonarensis sp. nov., a moderately haloalkaliphilic methylotroph isolated from the soda lake sediments of a meteorite impact crater Soda lakes represent extreme ecosystems and are characterized by their high pH and salinity (Grant & Jones, 2000). Unusually high primary productivity rates in such lakes are sustained mainly by prokaryotic communities that are actively involved in the closed cycling of organic matter (Zavarzin et al., 1999;Grant & Jones, 2000). Methane is a major end product of decomposition of organic matter in soda lakes, and methanotrophic bacteria have been identified as important biogeochemical agents that may drive alkaline methylotrophy by the production of C 1 compounds (methanol, formaldehyde and formate) (Trotsenko & Khmelenina, 2002). So far, only one haloalkaliphilic methylotrophic strain with a validly published name that possesses the ribulose monophosphate (RuMP) pathway has been reported from a soda lake environment: Methylophaga alcalica (Doronina et al., 2003). Very recently, the presence of novel Methylophaga-like methylotrophic bacteria was detected in the sediments of a saline and alkaline lake (Lonar Lake, Buldhana district, Maharashtra, India) by DNA-based stable isotope probing (SIP) with labelled methane and methanol (Antony et al., 2010). However, no haloalkaliphilic methylotroph has been isolated from Lonar Lake. Species of the genus Methylophaga differ from other RuMP-pathway methylotrophs in their requirements for high levels of Na + and Mg 2+, tolerance of NaCl and low DNA G+C content (Doronina et al., 2003;Boden, 2012).Surface sediment samples of high pH (pH 9.0-10.0) and moderate salinity (0.4-1.0 % NaCl) (Surakasi et al., 2007; Joshi et al., 2008) were collected from Lonar Lake. A 5 g sediment sample was incubated in sterile 120 ml serum vials for 2 weeks at 30 u C with 1 % (v/v) methane in the headspace. At regular intervals, the headspace gas was sampled and 3These authors contributed equally to this work.4Present address: School of Biomedical and Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK.1Present address:
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