Abstract:Microorganisms play a fundamental role in the cycling of nutrients and energy on our planet. A common strategy for many microorganisms mediating biogeochemical cycles in anoxic environments is syntrophy, frequently necessitating close spatial proximity between microbial partners. We are only now beginning to fully appreciate the diversity and pervasiveness of microbial partnerships in nature, the majority of which cannot be replicated in the laboratory. One notable example of such cooperation is the interspeci… Show more
“…For those cases, where the interaction partners have been studied in more detail, characteristic features such as the loss of essential biosynthetic functions (McInerney et al, 2007) or the formation of physical attachment structures (Ishii et al, 2005;Wanner et al, 2008) have been reported that may have arisen as specific adaptations to the symbiotic lifestyle. Unfortunately, the obligate interdependence of both partners makes it often difficult to study this type of interactions under laboratory conditions (Nauhaus et al, 2002;Pernthaler et al, 2008;McCutcheon and Moran, 2012). As a consequence, many open questions remain regarding the ecological and evolutionary consequences of entering into such an obligate cross-feeding interaction.…”
Cross-feeding interactions, in which bacterial cells exchange costly metabolites to the benefit of both interacting partners, are very common in the microbial world. However, it generally remains unclear what maintains this type of interaction in the presence of non-cooperating types. We investigate this problem using synthetic cross-feeding interactions: by simply deleting two metabolic genes from the genome of Escherichia coli, we generated genotypes that require amino acids to grow and release other amino acids into the environment. Surprisingly, in a vast majority of cases, cocultures of two cross-feeding strains showed an increased Darwinian fitness (that is, rate of growth) relative to prototrophic wild type cells-even in direct competition. This unexpected growth advantage was due to a division of metabolic labour: the fitness cost of overproducing amino acids was less than the benefit of not having to produce others when they were provided by their partner. Moreover, frequency-dependent selection maintained cross-feeding consortia and limited exploitation by non-cooperating competitors. Together, our synthetic study approach reveals ecological principles that can help explain the widespread occurrence of obligate metabolic cross-feeding interactions in nature.
“…For those cases, where the interaction partners have been studied in more detail, characteristic features such as the loss of essential biosynthetic functions (McInerney et al, 2007) or the formation of physical attachment structures (Ishii et al, 2005;Wanner et al, 2008) have been reported that may have arisen as specific adaptations to the symbiotic lifestyle. Unfortunately, the obligate interdependence of both partners makes it often difficult to study this type of interactions under laboratory conditions (Nauhaus et al, 2002;Pernthaler et al, 2008;McCutcheon and Moran, 2012). As a consequence, many open questions remain regarding the ecological and evolutionary consequences of entering into such an obligate cross-feeding interaction.…”
Cross-feeding interactions, in which bacterial cells exchange costly metabolites to the benefit of both interacting partners, are very common in the microbial world. However, it generally remains unclear what maintains this type of interaction in the presence of non-cooperating types. We investigate this problem using synthetic cross-feeding interactions: by simply deleting two metabolic genes from the genome of Escherichia coli, we generated genotypes that require amino acids to grow and release other amino acids into the environment. Surprisingly, in a vast majority of cases, cocultures of two cross-feeding strains showed an increased Darwinian fitness (that is, rate of growth) relative to prototrophic wild type cells-even in direct competition. This unexpected growth advantage was due to a division of metabolic labour: the fitness cost of overproducing amino acids was less than the benefit of not having to produce others when they were provided by their partner. Moreover, frequency-dependent selection maintained cross-feeding consortia and limited exploitation by non-cooperating competitors. Together, our synthetic study approach reveals ecological principles that can help explain the widespread occurrence of obligate metabolic cross-feeding interactions in nature.
“…Many studies have characterized the composition and ecological role of microorganisms in methanecontaining marine sediments around the world (Inagaki et al, 2006;Heijs et al, 2007;Parkes et al, 2007;Pernthaler et al, 2008;Wegener et al, 2008;Harrison et al, 2009;Hamdan et al, 2012). These works assist in understanding the biological controls on oceanic methane and may contribute to establishing baselines to monitor change in marine sediments.…”
Prokaryote communities were investigated on the seasonally stratified Alaska Beaufort Shelf (ABS). Water and sediment directly underlying water with origin in the Arctic, Pacific or Atlantic oceans were analyzed by pyrosequencing and length heterogeneity-PCR in conjunction with physicochemical and geographic distance data to determine what features structure ABS microbiomes. Distinct bacterial communities were evident in all water masses. Alphaproteobacteria explained similarity in Arctic surface water and Pacific derived water. Deltaproteobacteria were abundant in Atlantic origin water and drove similarity among samples. Most archaeal sequences in water were related to unclassified marine Euryarchaeota. Sediment communities influenced by Pacific and Atlantic water were distinct from each other and pelagic communities. Firmicutes and Chloroflexi were abundant in sediment, although their distribution varied in Atlantic and Pacific influenced sites. Thermoprotei dominated archaea in Pacific influenced sediments and Methanomicrobia dominated in methanecontaining Atlantic influenced sediments. Length heterogeneity-PCR data from this study were analyzed with data from methane-containing sediments in other regions. Pacific influenced ABS sediments clustered with Pacific sites from New Zealand and Chilean coastal margins. Atlantic influenced ABS sediments formed another distinct cluster. Density and salinity were significant structuring features on pelagic communities. Porosity co-varied with benthic community structure across sites and methane did not. This study indicates that the origin of water overlying sediments shapes benthic communities locally and globally and that hydrography exerts greater influence on microbial community structure than the availability of methane.
“…Another group, ANME-3, occurs for instance at Haakon Mosby Mud Volcano (Niemann et al, 2006; in situ temperature À1.5 1C) and the Eastern Mediterranean seepages (Omoregie et al, 2008;14 1C). Cells of both groups form dense consortia with specific bacterial phylotypes clustering with sulfate-reducing Deltaproteobacteria (most often within Desulfosarcinales, Seep-SRB-1a; Schreiber et al, 2010) or relatives of Desulfobulbus Lösekann et al, 2007;Pernthaler et al, 2008;Schreiber et al, 2010), respectively. A third phylogenetic group, ANME-1, is dominant in the microbial mats covering chimney structures at methane seeps in the Black Sea (Michaelis et al, 2002; in situ temperature of B10 1C), and in several diffusive methane interfaces (Thomsen et al, 2001;Lanoil et al, 2005;Harrison et al, 2009;Aquilina et al, 2010).…”
The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor. AOM is performed by microbial consortia of archaea (ANME) associated with partners related to sulfate-reducing bacteria. In vitro enrichments of AOM were so far only successful at temperatures p25 1C; however, energy gain for growth by AOM with sulfate is in principle also possible at higher temperatures. Sequences of 16S rRNA genes and core lipids characteristic for ANME as well as hints of in situ AOM activity were indeed reported for geothermally heated marine environments, yet no direct evidence for thermophilic growth of marine ANME consortia was obtained to date. To study possible thermophilic AOM, we investigated hydrothermally influenced sediment from the Guaymas Basin. In vitro incubations showed activity of sulfate-dependent methane oxidation between 5 and 70 1C with an apparent optimum between 45 and 60 1C. AOM was absent at temperatures X75 1C. Long-term enrichment of AOM was fastest at 50 1C, yielding a 13-fold increase of methane-dependent sulfate reduction within 250 days, equivalent to an apparent doubling time of 68 days. The enrichments were dominated by novel ANME-1 consortia, mostly associated with bacterial partners of the deltaproteobacterial HotSeep-1 cluster, a deeply branching phylogenetic group previously found in a butane-amended 60 1C-enrichment culture of Guaymas sediments. The closest relatives (Desulfurella spp.; Hippea maritima) are moderately thermophilic sulfur reducers. Results indicate that AOM and ANME archaea could be of biogeochemical relevance not only in cold to moderate but also in hot marine habitats.
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