Complex nitrogen cycling in the sponge Geodia barretti

Abstract

Marine sponges constitute major parts of coral reefs and deep-water communities. They often harbour high amounts of phylogenetically and physiologically diverse microbes, which are so far poorly characterized. Many of these sponges regulate their internal oxygen concentration by modulating their ventilation behaviour providing a suitable habitat for both aerobic and anaerobic microbes. In the present study, both aerobic (nitrification) and anaerobic (denitrification, anammox) microbial processes of the nitrogen cycle were quantified in the sponge Geodia barretti and possible involved microbes were identified by molecular techniques. Nitrification rates of 566 nmol N cm(-3) sponge day(-1) were obtained when monitoring the production of nitrite and nitrate. In support of this finding, ammonia-oxidizing Archaea (crenarchaeotes) were found by amplification of the amoA gene, and nitrite-oxidizing bacteria of the genus Nitrospira were detected based on rRNA gene analyses. Incubation experiments with stable isotopes ((15)NO(3)(-) and (15)NH(4)(+)) revealed denitrification and anaerobic ammonium oxidation (anammox) rates of 92 nmol N cm(-3) sponge day(-1) and 3 nmol N cm(-3) sponge day(-1) respectively. Accordingly, sequences closely related to 'Candidatus Scalindua sorokinii' and 'Candidatus Scalindua brodae' were detected in 16S rRNA gene libraries. The amplification of the nirS gene revealed the presence of denitrifiers, likely belonging to the Betaproteobacteria. This is the first proof of anammox and denitrification in the same animal host, and the first proof of anammox and denitrification in sponges. The close and complex interactions of aerobic, anaerobic, autotrophic and heterotrophic microbial processes are fuelled by metabolic waste products of the sponge host, and enable efficient utilization and recirculation of nutrients within the sponge-microbe system. Since denitrification and anammox remove inorganic nitrogen from the environment, sponges may function as so far unrecognized nitrogen sinks in the ocean. In certain marine environments with high sponge cover, sponge-mediated nitrogen mineralization processes might even be more important than sediment processes.

Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis

“…This suggests that specific pathways and regulation of assimilation are preferred in the sponge-associated community and that assimilation processes rather than oxidation might be important for the ammonium utilization by the bacterial community in C. concentrica. In addition, anaerobic pathways such as sulphate reduction, denitrification or anammox, which have been described in deep-water sponge systems (Hoffmann et al, 2009;Bruck et al, 2010), are not abundant in the C. concentrica metagenome, which is consistent with the thin structure of this shallow-water sponge's being unlikely to experience anaerobiosis.…”

Host-specificity among abundant and rare taxa in the sponge microbiome

“…and in the seawater samples, suggesting that these nitrite-oxidizing bacteria may serve a key role in removing ammonia that accumulates in Hexadella sp. In contrast, the restricted amount of Nitrospira in Mycale suggests that another member of the community may perform nitrification in this species or that other specific pathways (for example, sulfate reduction, denitrification or anammox, described in species experiencing anaerobiosis, see Hoffmann et al, 2009) might provide greater fitness to Mycale sp. The relative abundance of Nitrospira in Hexadella spp compared with other sponge species (that is, Mycale) suggests that this particular genera specifically occurs in certain sponge species.…”

Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone

“…Thus, in low-oxygen environments, they potentially can compete for ammonia, or interact with AOA, providing nitrite to anammox bacteria. Indeed, anammox bacteria and AOA have been reported to co-exist in the same water masses in the Black Sea (Kuypers et al, 2003;Francis et al, 2005;Coolen et al, 2007), in marine sponges (Hoffmann et al, 2009) and in suspended particles in the Namibian upwelling system (Woebken et al, 2007). In addition, Lam et al (2007) presented evidence that AOA together with nitrifying bacteria provide nitrite for anammox bacteria in the Black Sea.…”