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 reports, 6. https://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 Microbiology, 10(11), 2942-2955. http://onlinelibrary.wiley.com/doi/10.1111/j.1462-2920.2008.01582.x/full
Davis,
ReplyDeleteReally 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
Hi Scott,
ReplyDeleteThanks 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