Saturday 8 October 2016

SpongeNOB SquarePants: Microbial Nitrification in a Marine Sponge

Microbes are essential to the cycling of nitrogenous compounds in ocean systems. The process of nitrification involves the oxidation of ammonia to bioavailable nitrate via a nitrite intermediary. Ammonia can exist in marine environments as a fixation product of diazotrophic cyanobacteria, however a large source is attributable to the nitrogenous waste of various organisms. Sponges excrete ammonia as a waste product however there is evidence to suggest that this waste is detoxified by the metabolic activity of the sponge microbiome. Previous metagenomic studies (such as Bayer et al, 2008) identified 16S rRNA genetic signatures of nitrifying microbiota in marine sponges. This implies that the filtration activities of sponges may play a key biochemical role in the nitrification of regional waters. However, transcriptional data for such species is lacking and therefore the functional nitrifying activity of these microbes is poorly understood.

To rectify this, Feng et al, 2016 applied gene-sequencing and transcriptional profiling to the nitrifying microbiome of the widely distributed sponge Theonella swinhoei (Porifera: Demospongiae) collected from the South China Sea. The authors characterised the community identity by PCR amplification of 16S rRNA and microbial nitrification gene sequences using targeted primers. Subsequent phylogenetic analyses revealed that archaeal 16S rRNA and amoA amplicons (the latter coding for a subunit of ammonia monooxygenase) were closely related to Nitrosopumilus-like ammonia-oxidising Archaea (AOA) while bacterial 16S rRNA and nxrB amplicons (the latter coding for a subunit of nitrite oxidoreductase) were closely related to Nitrospira-like nitrite-oxidising Bacteria (NOB). Interestingly, the authors went on to quantify the relative abundance of these taxa and found AOA’s to be significantly more prevalent than NOB’s, which correlated to the increased relative abundance of AOA amoA to NOB nxrB mRNA as measured using qPCR. The authors hypothesise that the abundance of AOA is attributable to the importance of ammonia detoxification in maintaining the health of the sponge. Overall, this study provides a key insight into nitrification within a model sponge holobiont. Previous studies have exemplified the importance of marine microbes in global nitrification (such as Karner et al, 2001), however it appears that similar processes govern regional and intra-organismal nitrification.

However, there should be caution in extrapolating these findings too broadly. Even at an intraspecific scale, the AOA and NOB community structure identified in this study is incongruent with that characterised from an allopatric Palau population of the same species. This suggests that idiosyncrasies are rife in the sponge holobiont, attributable to either biogeographically differential abiotic factors or host selection of microbiota.

In the future, I would like to see this study embellished with mesocosmic studies, perhaps using the nitrification inhibitor nitrapyrin to gain a greater understanding of sponge nitrification as a phenotype.  I would also be excited to see these findings augmented with further research into the diversity and genetic repertoire of denitrifying sponge-associated Bacteria. As sponges possess the ability to filter vast volumes of water, a comprehensive understanding of such Bacteria may enable researchers to exploit this ability in the bioremediation of eutrophicated waters.


In conclusion, this research should be appreciated as a fascinating case study into microbial nitrification within a sponge holobiont but cannot at this stage represent a generalisation. Its significance should not be exaggerated until further research is conducted.  

Reviewed Paper: Feng, G., Sun, W., Zhang, F., Karthik, L., & Li, Z. (2016). Inhabitancy of active Nitrosopumilus-like ammonia-oxidizing archaea and Nitrospira nitrite-oxidizing bacteria in the sponge Theonella swinhoei. Scientific reports6https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4844951/

Further Reading: Bayer, K., Schmitt, S., & Hentschel, U. (2008). Physiology, phylogeny and in situ evidence for bacterial and archaeal nitrifiers in the marine sponge Aplysina aerophoba. Environmental Microbiology10(11), 2942-2955. http://onlinelibrary.wiley.com/doi/10.1111/j.1462-2920.2008.01582.x/full

2 comments:

  1. Davis,

    Really interesting post and I thoroughly enjoyed your thoughts on the topic. At the end of your blog you mention that a better understanding of sponge associated bacteria may enable researchers to exploit the denitrifying ability as a method of bioremediation in eutrophicated waters as sponges filter large volumes of water. As you may know the sponge T. swinhoei is known to actively uptake large concentrations of arsenic from the environment (Mayzel et al., 2014) and the associated bacteria are thought to play a large role in this. These bacteria are hypothesised to have adapted to the arsenic rich internal environment of their sponge host and are integral to the natural arsenic cycle.

    You mention that 'microbes are essential to the cycling of nitrogenous compounds in the ocean systems', I would be interested to know your thoughts on not just nitrification but other ways in which sponges and their associated bacteria affect ocean systems?

    Cheers
    Scott

    Keren, Ray et al. "Culturable Associated-Bacteria Of The Sponge Theonella Swinhoei Show Tolerance To High Arsenic Concentrations". Frontiers in Microbiology 6 (2015): n. pag. Web.

    Mayzel, B., Aizenberg, J., and Ilan, M. (2014). The elemental composition of demospongiae from the Red Sea, Gulf of Aqaba. PLoS ONE 9:e95775. doi: 10.1371/journal.pone.0095775

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  2. Hi Scott,

    Thanks for your comment. I was unaware of the research into As-accumulation in sponge microbiota so thank you for bringing that to my attention. It has also previously been shown that sponge-associated microbial symbionts can accumulate PO4 in the form of polyphosphate granules, essential to nutrient cycling in oligotrophic waters (Zhang et al, 2015) and PCR-DGGE fingerprinting reveals the potential of such bacteria to tolerate a range of toxic heavy metals (Bauvais et al, 2015). Forest Rohwer has written much about the importance of viewing coral reefs as ‘holobionts’ – a synthesis of the metazoan host and its associated microbiome. I feel sponges deserve the same treatment. It is the ability of sponge choanocytes to circulate vast quantities of water through their feeding chambers, however it is becoming more apparent that much of the biochemical flexibility of sequestration and bioremediation potential is attributable to associated microbiota. That is why a comprehensive understanding of the intricacies of the sponge holobiont is necessary to gain an accurate ecological and biogeochemical understanding. Interestingly, the population of T. swinhoei used in Keren et al 2015 was from the Red Sea and, considering the differences in bacterial community composition highlighted in the study I reviewed, I wonder if the As-accumulating ability would hold true for the South China Sea population? Abiotic and population variables must be studied further.

    Thanks,
    Davis

    Zhang, F., Blasiak, L. C., Karolin, J. O., Powell, R. J., Geddes, C. D., & Hill, R. T. (2015). Phosphorus sequestration in the form of polyphosphate by microbial symbionts in marine sponges. Proceedings of the National Academy of Sciences, 112(14), 4381-4386. http://www.pnas.org/content/112/14/4381.short

    Bauvais, C., Zirah, S., Piette, L., Chaspoul, F., Domart-Coulon, I., Chapon, V., ... & Bourguet-Kondracki, M. L. (2015). Sponging up metals: bacteria associated with the marine sponge Spongia officinalis. Marine environmental research, 104, 20-30. http://www.sciencedirect.com/science/article/pii/S0141113614002098

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