Distribution and Diversity of Archaeal Ammonia Monooxygenase Genes Associated with Corals

Beman, J. Michael; Roberts, Kathryn; Wegley, Linda; Rohwer, Forest; Francis, Christopher A.

doi:10.1128/aem.00461-07

Cited by 113 publications

(100 citation statements)

References 49 publications

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“…Single-cell view of ammonium assimilation in corals M Pernice et al nitrite to nitrate that could be then assimilated by the coral host (Mohideen et al, 1990;Beman et al, 2007). A few localized 15 N-enrichment 'hotspots' were detected in the host epiderm, which could reflect the activity of such microbial communities.…”

Section: Resultsmentioning

confidence: 99%

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

et al. 2012

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Assimilation of inorganic nitrogen from nutrient-poor tropical seas is an essential challenge for the endosymbiosis between reef-building corals and dinoflagellates. Despite the clear evidence that reef-building corals can use ammonium as inorganic nitrogen source, the dynamics and precise roles of host and symbionts in this fundamental process remain unclear. Here, we combine high spatial resolution ion microprobe imaging (NanoSIMS) and pulse-chase isotopic labeling in order to track the dynamics of ammonium incorporation within the intact symbiosis between the reefbuilding coral Acropora aspera and its dinoflagellate symbionts. We demonstrate that both dinoflagellate and animal cells have the capacity to rapidly fix nitrogen from seawater enriched in ammonium (in less than one hour). Further, by establishing the relative strengths of the capability to assimilate nitrogen for each cell compartment, we infer that dinoflagellate symbionts can fix 14 to 23 times more nitrogen than their coral host cells in response to a sudden pulse of ammoniumenriched seawater. Given the importance of nitrogen in cell maintenance, growth and functioning, the capability to fix ammonium from seawater into the symbiotic system may be a key component of coral nutrition. Interestingly, this metabolic response appears to be triggered rapidly by episodic nitrogen availability. The methods and results presented in this study open up for the exploration of dynamics and spatial patterns associated with metabolic activities and nutritional interactions in a multitude of organisms that live in symbiotic relationships.

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Section: Resultsmentioning

confidence: 99%

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

et al. 2012

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“…The rare bacterial classes showing clear evidence of enrichment in the backreef relative to offshore waters included a number of groups containing potential pathogens of Metazoa (Bacilli, Clostridia, Actinobacteria, Bacteroidia, Sphingobacteria), as well as several groups associated more with environmental samples or specific redox transformations (Acidobacteria, Nitrospira, Fusobacteria, Verrucomicrobia, Planctomycetes and Lentisphaeria). Elevated levels of nitrifying bacteria have been reported in other reef habitats (Beman et al, 2007;Wegley et al, 2007) and may provide a mechanism explaining the elevated winter concentrations of nitrate in the backreef (Supplementary Figure S2). The three reef water column environments sampled by pyrosequencing (forereef, backreef: lagoon and backreef: fringe) showed markedly higher numbers of bacterial OTUs for equal sampling intensity (sequence reads) compared with offshore and bay habitats (Supplementary Table S1).…”

Section: Discussionmentioning

confidence: 99%

Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem

et al. 2011

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Coral reefs are highly productive ecosystems bathed in unproductive, low-nutrient oceanic waters, where microbially dominated food webs are supported largely by bacterioplankton recycling of dissolved compounds. Despite evidence that benthic reef organisms efficiently scavenge particulate organic matter and inorganic nutrients from advected oceanic waters, our understanding of the role of bacterioplankton and dissolved organic matter (DOM) in the interaction between reefs and the surrounding ocean remains limited. In this study, we present the results of a 4-year study conducted in a well-characterized coral reef ecosystem (Paopao Bay, Moorea, French Polynesia) where changes in bacterioplankton abundance and dissolved organic carbon (DOC) concentrations were quantified and bacterial community structure variation was examined along spatial gradients of the reef:ocean interface. Our results illustrate that the reef is consistently depleted in concentrations of both DOC and bacterioplankton relative to offshore waters (averaging 79 lmol l À1 DOC and 5.5 Â 10 8 cells l À1 offshore and 68 lmol l À1 DOC and 3.1 Â 10 8 cells l À1 over the reef, respectively) across a 4-year time period. In addition, using a suite of culture-independent measures of bacterial community structure, we found consistent differentiation of reef bacterioplankton communities from those offshore or in a nearby embayment across all taxonomic levels. Reef habitats were enriched in Gamma-, Delta-, and Betaproteobacteria, Bacteriodetes, Actinobacteria and Firmicutes. Specific bacterial phylotypes, including members of the SAR11, SAR116, Flavobacteria, and Synechococcus clades, exhibited clear gradients in relative abundance among nearshore habitats. Our observations indicate that this reef system removes oceanic DOC and exerts selective pressures on bacterioplankton community structure on timescales approximating reef water residence times, observations which are notable both because fringing reefs do not exhibit long residence times (unlike those characteristic of atoll lagoons) and because oceanic DOC is generally recalcitrant to degradation by ambient microbial assemblages. Our findings thus have interesting implications for the role of oceanic DOM and bacterioplankton in the ecology and metabolism of reef ecosystems.

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“…The contributions of planktonic and sediment microbial communities to the marine nitrogen cycle is well appreciated (32), but only recently have studies revealed a high rate of nitrogen metabolism in marine microorganisms associated with invertebrate hosts, especially the reef-building corals and sponges (33)(34)(35). Nitrogen fixation (36), nitrification (37,38), anaerobic respiration of ammonium (anammox) (38), and denitrification (38,39) activities have been analyzed separately in various marine sponges by stable isotope probing or 16S rRNA or functional gene analyses.…”

Section: Functional Annotation Reveals Shared Genomic Signatures In Smentioning

confidence: 99%

Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts

Fan

Reynolds

Liu

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

329

465

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Microorganisms often form symbiotic relationships with eukaryotes, and the complexity of these relationships can range from those with one single dominant symbiont to associations with hundreds of symbiont species. Microbial symbionts occupying equivalent niches in different eukaryotic hosts may share functional aspects, and convergent genome evolution has been reported for simple symbiont systems in insects. However, for complex symbiont communities, it is largely unknown how prevalent functional equivalence is and whether equivalent functions are conducted by evolutionarily convergent mechanisms. Sponges represent an evolutionarily divergent group of species with common physiological and ecological traits. They also host complex communities of microbial symbionts and thus are the ideal model to test whether functional equivalence and evolutionary convergence exist in complex symbiont communities across phylogenetically divergent hosts. Here we use a sampling design to determine the phylogenetic and functional profiles of microbial communities associated with six sponge species. We identify common functions in the six microbiomes, demonstrating the existence of functional equivalence. These core functions are consistent with our current understanding of the biological and ecological roles of sponge-associated microorganisms and also provide insight into symbiont functions. Importantly, core functions also are provided in each sponge species by analogous enzymes and biosynthetic pathways. Moreover, the abundance of elements involved in horizontal gene transfer suggests their key roles in the genomic evolution of symbionts. Our data thus demonstrate evolutionary convergence in complex symbiont communities and reveal the details and mechanisms that underpin the process.

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Distribution and Diversity of Archaeal Ammonia Monooxygenase Genes Associated with Corals

Cited by 113 publications

References 49 publications

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem

Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts

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