Oil and
water don’t mix. Due to its low density and extreme hydrophobicity, crude oil
from anthropogenic oil disasters forms a surface-associated slick and it is
here that remediation efforts are concentrated. However, the formation of
so-called ‘tarballs’ and the incorporation of oil into marine snow means that a
significant fraction is exported to deep-sea habitats. The genus Alcanivorax holds a reputation as a
globally important microbial hydrocarbon-degrader, and can constitute >80%
of the bacterial community during oil spills. Interestingly, Alcanivorax congeners are conspicuously absent from deep-sea environments.
Microbial surveys concerning the fate of deep-sea oil from the Deepwater
Horizon oil spill (2010) highlighted a paucity of Alcanivorax signatures which was intriguing, considering the
dominance of the genus in surface waters. It is possible that the intense
hydrostatic pressure of the ocean depths somehow impairs the growth and physiology
of Alcanivorax however this
hypothesis lacks support. Scoma and colleagues (2016) therefore examined the
validity of this idea.
Cultures of
the genus type strain (Alcanivorax
borkumensis SK2) were grown under 0.1, 5 or 10 MPa (equating to 0, 500 and
1000m of SW respectively) with the hydrocarbon n-dodecane as the sole carbon source. Unsurprisingly, growth at 5
MPa was heavily impaired relative to 0.1 MPa. Strikingly, however, growth was slightly
higher at 10 MPa relative to 5 MPa and 10 MPa cultures exhibited a higher
proportion of intact cells. This lead the authors to hypothesise that SK2 must
express resistance mechanisms under higher extremes of hydrostatic pressure. Subsequent
RNA-Seq of the 10MPa transcriptome revealed that, while total gene expression
was lower than at 0.1 MPa, central metabolic pathways (e.g protein translation,
ribosomal biogenesis and coenzyme metabolism) were upregulated. As well as
this, the authors identified a 10-fold higher concentration of the nitrogenous
osmolyte ectoine in 10 MPa cultures. While increased ectoine biosynthesis has
been previously associated with increasing salinity, this the first report of
ectoine as a piezolyte, which offers a thrilling area for further study into
how widespread this phenomenon is. Based on this, the authors conclude that,
while A. borkumensis lacks proper
adaptation to high hydrostatic pressure, certain physiological mechanisms can
confer limited resistance. Therefore, hydrostatic pressure may represent a
driver in the vertical distribution of Alcanivorax.
This study
offers a controlled and elegant approach to exploring the effect of hydrostatic
pressure on the growth and physiology of an Alcanivorax
species. However, like all univariate laboratory studies, one should be
cautious in extrapolating too heavily into an ecological framework. For
example, as the majority of hydrocarbons are surface-bound it may be that those
which are transported to deeper waters are recalcitrant and less available to Alcanivorax congeners than at the
surface. Also, we cannot omit ecological competition and niche exclusion from
any explanation. Other studies simulating oil spills in the Gulf of Mexico,
such Baelum et al, 2012, have shown
that other hydrocarbonoclastic Bacteria
(such as Colwellia) are enriched in
deep-sea sediments during oil spills and therefore exclusion by deeper adapted
species may play a contributory role.
Nevertheless,
this research provides a reasonable explanation as to why the distribution of Alcanivorax is limited by depth. Further
research into the mechanisms of hydrostatic adaption in deep-sea
hydrocarbonoclastic Bacteria would
greatly benefit efforts to bioremediate oil spills in deep-sea sediments.
Reviewed
Paper: Scoma, A., Barbato, M., Borin, S., Daffonchio, D., & Boon, N.
(2016). An impaired metabolic response to hydrostatic pressure explains
Alcanivorax borkumensis recorded distribution in the deep marine water column.
Scientific Reports, 6. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4981847/
Deep-Sea Microbes: Bælum, J., Borglin, S., Chakraborty, R., Fortney, J. L., Lamendella, R., Mason, O. U., ... & Malfatti, S. A. (2012). Deep‐sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environmental microbiology, 14(9), 2405-2416. http://onlinelibrary.wiley.com/doi/10.1111/j.1462-2920.2012.02780.x/full
Hi Davis,
ReplyDeleteThis is a really interesting review but I agree that much more research would be needed for Alcanivorax to be considered as a tool for removing oil from deep sea sediments. It would be interesting to see at exactly what pressure the bacteria begin implementing these resistance mechanisms.
Do you think there would be some kind of trade off between pressure resistance and some other physiological trait?
A lot of recalcitrant carbon accumulates in the deep sea - can any of the deeper adapted species actually break this down, or do they only use labile carbon from recent oil spills and other sources?
Thanks, Tabby
Hi Tabby,
ReplyDeleteThanks for your comment. You raise some great points – in regards to potential tradeoffs, I think there very well may be some. The transcriptomic data suggests that the 10 MPa cultures had reduced expression of the majority (56%) of their genes, so it appears that diverse physiological processes are downregulated to focus on central metabolic pathways. It is important to note that, while these resistance mechanisms are interesting, the fitness of the 10 MPa cultures was still considerably lower than the ‘surface’ control. I completely agree that it is would be fascinating to find out at what pressure this is triggered and whether that has ecological ramifications.
In regards to recalcitrant hydrocarbon degradation as a distribution driver, I cannot be sure and it was merely an alternate hypothesis that I put forward. However, as stated in Michael’s lecture (18/11/16), chemical profiling here in Plymouth by Prof. Steve Rowland has shown that crude oil is a diverse and sometimes unresolved mixture of compounds, so it may very well be the case that hydrocarbonoclastic Bacteria dominate different chemical niches. I came across this terrestrial example that describes the isolation of a hexane-degrading bacterium, Rhodococcus sp. EH831, that can degrade hexane (a recalcitrant hydrocarbon) faster than any previous isolate at the time:
Lee, E. H., Kim, J., Cho, K. S., Ahn, Y. G., & Hwang, G. S. (2010). Degradation of hexane and other recalcitrant hydrocarbons by a novel isolate, Rhodococcus sp. EH831. Environmental Science and Pollution Research, 17(1), 64-77. http://link.springer.com/article/10.1007/s11356-009-0238-x
We also know that Alcanivorax (unsurprisingly) specialises in alkane degradation whereas Cycloclasticus degrades aromatics (Harayama et al, 2004). I think the microbe-microbe interactions between such species stratified across chemical niches merits further investigation.
Hope that helps,
Davis
Harayama, S., Kasai, Y., & Hara, A. (2004). Microbial communities in oil-contaminated seawater. Current opinion in biotechnology, 15(3), 205-214. http://www.sciencedirect.com/science/article/pii/S0958166904000540