Boronated tartrolon antibiotic produced by symbiotic cellulose-degrading bacteria in shipworm gills
J. Hinchcliffe
Shipworms rely on gill symbionts to survive in their habitat, they are well known for the ability to burrow into wood. As in other animals that consume wood, it is thought that the shipworm’s microbial symbionts facilitate the degradation of cellulose, which without the presence of microbial symbionts the animal is unable to digest. Teredinibacter turnerae, a symbiont species, has been isolated from different shipworm hosts collected around the world; it secretes wood degrading enzymes thought to assist the host indigestion. An interesting point is that the symbiotic bacteria live in the gill but cellulose is degraded in the digestive tract in the cecum. Although the gut is an excellent habitat for microbes in organisms, the cecum in shipworms contains very few bacteria. This absence is striking, because cellulose digestion increases the availability of glucose, which is an excellent nutrient source for microbes. The genome of one strain, T. turnerae T7901, was sequenced and revealed, in addition to genes that encode enzymes specific for lignocellulose degradation and nitrogen fixation, at least nine regions encode enzymes for the biosynthesis of polyketides and nonribosomal peptides.
Elshahawi et al (2013) therefore hypothesized that some of the secondary metabolites produced by T. turnerae might contribute to reducing the bacterial population in the cecum to prevent glucose scavenging and that secondary metabolites might play a significant role in microbial competition among symbionts in the gill. Elshahawi and co described the polyketide tartrolons, antibiotics that are produced by T. turnerae that were detected in shipworms. These and other antibiotics from shipworm symbionts may help structure the symbiont community, possibly even enabling the unique lignocellulose digestion strategy found in shipworms. This study reports the secondary metabolites identified from T. turnerae and their bioactivities, describes the biosynthetic gene cluster linked to them, and presents evidence that these metabolites are produced in the symbiotic state.
In summary, Elshahawi et al identified two molecules called macro diolides from the marine shipworm symbiont T. turnerae T7901, that had anti-bacterial activity. They also identified a biosynthetic gene cluster that will shed more light on the biosynthesis of other active natural products in this class. Moreover, tartrolons were detected in the shipworm host and in other T. turnerae strains, which suggests that it plays a role in the bioactive metabolite symbiosis of the shipworm.
So in my opinion….. T. turnerae plays a major role in the shipworm symbiosis. Its genome contains information enabling this bacterium to have a facultative endosymbiotic or even a free-living lifestyle, yet T. turnerae has only been found in intracellular symbiotic association with the molluscs. The trt gene cluster that was found in this investigation has a potential role in the shipworm–microbial symbiosis. The antibacterial macrodiolides produced by the shipworm symbionts in the gills might contribute to bacterial suppression in the cecum, this suppression could allow the host to maximize efficient uptake of the glucose liberated by the breakdown of lignocellulose. But the mechanism by which products of the symbionts in the gill could be translocated to the cecum is unknown. How do the symbionts get in the microbes in the first place? Much remains unknown but I feel this study contributes significantly to the field.
Hi James,
ReplyDeleteFascinating stuff, I’m really interested in the mechanisms of symbiosis relationships so reading your post has been great. So the tartrolon antibiotic (AB) compounds they isolated, are they broad or narrow spectrum? I wonder if the AB compound not only reduces glucose scavenging by other microbes (as suggested in your blog), but also could provide the host with protection against pathogens… In this way both the host and the symbiont are benefiting. Did the paper provide any alternative explanations apart from prevention of glucose scavenging by other microbes?
Thanks,
Vicky
Hi Vickie, thank you for showing an interest.
ReplyDeleteSorry I may have been a little too concise in my blog.
Ok so in their discussion, Elshahawi et al (2013) list some examples that have been reported with a wide spectrum but do not directly mention this in the text (from what I can gather anyways).
So are there any alternative explanations apart from prevention of glucose scavenging by for the results? I missed out quite a large chunk of this in my blog due to word count constraints, however now that you have asked the question…
The study mentions that shipworm symbionts previously have been shown to contribute to nitrogen metabolism in the host and have been proposed to contribute to lignocellulose digestion. However their potential function as producers of secondary metabolites has yet to be fully explored. The authors also mentioned that another study by Pérez et al. (9) identified one of the macro diolide compounds isolated here, I have skipped a lot of biochemistry description but basically the compound was found from a marine actinomycete species that is phylogenetically distant from the Gammaproteobacteria T. turnerae (the symbiont used in this investigation). This group of compound overall (the macro diolides) are well-known for their pharmacological activities; presumably the antibacterial activities as in this study both compounds 1 and 2 inhibited B. subtilis. Moreover, compound 2 inhibited the growth of the marine pathogen V. anguillarum and a shipworm Bankia setacea isolate, BS02, but not the eukaryote C. albicans. This suggests that the compounds play a could play a role in microbial competition in the shipworm system by targeting opportunistic bacteria. Compound 2 possessed a deterrent activity against certain members of the symbiont community but not others, so this led the authors to speculate that this could maintain a population of similar strain.
Another interesting explanation is that the 2 compounds have an ability to bind to boron. Again I must emphasise I have skipped some biochemistry to make explaining a bit more simple. But basically boron exists in the form of borate or orthoborate in the oceans and is known to play important roles in living organisms but is toxic at high levels. The 2 compounds could play an important role in the transport of boron as boron transporters have been reported from other living organisms. No homologs for borate transporters were detected in this study but some microorganisms have evolved biosynthetic pathways to acquire iron in the form of siderophores. So organisms that lack the ability to express boron transporters might have evolved multi-functional molecules that facilitate boron transport or even exclude toxic levels. Given that the concentration of boron in the ocean is estimated to be 400 μM, rather high according to the authors, the expression of compounds 1 and 2 found here in the study might give ship worms a control mechanism either to decrease its toxicity or to make use of its abundance. So is also is possible that the 2 macro diolide compounds isolated in this study have multiple functions, acting as both as an antibacterial and as a boron transporter in the shipworm system.
Thanks again for asking, hope that helps
James
Cheers James, I asked about the spectrum of the ABs as this kind of knowledge could help our understanding of function so it seems strange the authors didn’t discuss this. From your further explanation it appears the possible functional explanations are endless. Maybe the authors will peruse some more experimental work in order to reveal the adaptive function of these ABs, I agree it is likely they have multiple functions benefiting both host and the symbiont.
ReplyDeleteThanks ,
Vicky