by Joseph A. Christie-Oleza and Vinko Zadjelovic
Cleaners of the ocean
The first image that comes to our mind when we think of the oceans is immense bodies of clear waters or – in the more 'romantic' minds – beautiful turquoise waters that caress tropical beaches. Such clear waters come as a consequence of the extreme lack of nutrients in these ecosystems. Nevertheless, the elevated primary productivity measured in seawater, which produces half of the oxygen we breathe, highlights the efficient use and rapid turnover of nutrients in these systems. Nothing goes to waste… until our waste gets in the way. How do such optimised microbiomes deal with anthropogenic pollutants?
These pollutants are often aliphatic hydrocarbons, the major components of plastics and large portions of crude oil, for example alkanes. Fortunately, marine ecosystems contain expert microbial degraders for such compounds. This 'brigade of microbial cleaners' is composed of obligate hydrocarbonoclastic bacteria (OHCB). Of the handful of microbial genera included in this group, Alcanivorax is by far the most studied and well known. While normally present at very low abundance under pristine conditions, these specialised biodegraders flourish when exposed to such pollutants (others like the Psychrobacters were just recently featured in STC.)
But how does Alcanivorax persist under pristine conditions? Initial thoughts were that they remained dormant awaiting for a polluting event in order to bloom. Now we know that marine cyanobacteria – numerically the most abundant phototrophs on Earth – produce alkanes that can keep the small populations of OHCB alive and active around the globe.
Biodegradation of oil… and plastics!?
Alcanivorax and other OHCBs degrade alkanes using different kinds of monooxygenases: AlkB, cytochrome P450 and the flavin-containing monooxygenase AlmA, able to degrade long-chain alkanes (>C20; Figure 1). These monooxygenases oxidize the alkanes that are then funnelled into the fatty acid β-oxidation pathway. Crude oil mainly contains medium- and long-sized alkanes (C5–C35), but some synthetic polyolefin polymers such as polyethylene are thousands of carbon atoms long, being 'just' incredibly-long alkanes. Polyethylene is no joke, it represents 30% of global plastic production and, being less dense than water, it is also the most abundant plastic found floating in the oceans. Due to the chemical similarity between alkanes and polyethylene, it is not surprising that researchers have speculated that OHCBs might degrade this and other polyolefin plastics. In fact, the recurrent identification of such bacteria on biofilms growing on marine plastic debris – the Plastisphere – is an indicator of potential plastic biodegradation. Nevertheless, the mechanistic understanding of such a process and robust proof of plastic biodegradation by OHCBs is still underway.
We found that, in addition to degrading alkanes, many strains of Alcanivorax can also efficiently degrade natural and synthetic aliphatic polyesters. For this, these bacteria produce and secrete large amounts of a broad-range esterase that cuts these polymeric chains, making the hydrolysed subunits available for consumption. Natural polyesters, for example polyhydroxyalkanoates, are common carbon storage polymers that many microbes accumulate when nutrients, such as phosphorus, are scarce. Hence, this natural polymer – that may be released during phage attack, inefficient grazing or cell death – is an additional source of carbon and energy that may keep Alcanivorax active in pristine seawater. But the esterase secreted by Alcanivorax can also break down synthetic aliphatic polyesters, that is. polybutylene succinate, polyethylene succinate and polycaprolactone (Figure 3). These aliphatic polyesters are considered biodegradable alternatives to recalcitrant plastics and, with Alcanivorax populating marine environments, we now know the potential for biodegrading these more eco-friendly materials already exists in oceanic ecosystems.
Hence, in addition to oil spill bioremediation, we may also need to thank the genus Alcanivorax and other OHCBs for marine plastic pollution clean-up. Nevertheless, while the involvement of this incredibly specialised hydrocarbon biodegrader has been proven for aliphatic polyesters, its involvement in traditional plastic degradation remains elusive. The full picture of the contribution of Alcanivorax as a versatile degrader of marine pollution is certainly a matter of further research!