In:
Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, Vol. 109, No. 19 ( 2012-05-08)
Abstract:
Our results show that a large proportion of the proteins expressed in the O. algarvensis symbiosis are involved in nutrient and energy uptake and conservation. This finding suggests that the organisms’ impoverished environment exerts a strong selective pressure for metabolic pathways that maximize these processes. Some of the metabolic strategies used by the O. algarvensis symbionts also appear to play an important role in free-living bacteria such as planktonic SAR11 bacteria from low-nutrient ocean waters that express high-affinity uptake transporters at high abundances similar to those of the O. algarvensis δ-symbionts ( 5 ). Furthermore, our comparative analyses of the genes used by the O. algarvensis symbionts for energy-efficient pathways revealed that these genes appear to be widespread in free-living chemoautotrophic and sulfate-reducing bacteria. Thus, our study shows that the O. algarvensis symbiosis is an excellent model system for understanding how life has evolved to survive environments with low nutrient and energy availability. We identified and quantified 2,819 proteins and 97 metabolites in the O. algarvensis symbiosis. The identified proteins included 530 proteins from the host, thus providing insight into the metabolism of a marine oligochaete, a group of segmented annelid worms for which no genomic data are available. Our analyses revealed ( i ) multiple symbiont pathways for the recycling of host waste products, including a pathway for the assimilation of acetate, propionate, succinate, and malate; ( ii ) the potential use of carbon monoxide as an energy source, a substrate previously not known to play a role in marine invertebrate symbioses; ( iii ) the potential use of hydrogen as an energy source; ( iv ) the extremely abundant expression of high-affinity uptake transporters that allow the uptake of a wide range of substrates at very low concentrations; and ( v ) as yet undescribed energy-efficient steps in CO 2 fixation and sulfate reduction involving pyrophosphate-dependent enzymes. We developed a method called “proteomics-based binning” to decipher metabolic pathways and identify the symbiont from which they originated. Our goal was to understand the functional roles of the different symbiotic partners and their interactions within the symbiosis. Further, we aimed to identify the metabolic pathways that could explain how O. algarvensis is able to thrive in its oligotrophic habitat. In this study, we used various analytical methods to gain an in-depth understanding of the intricate interactions between O. algarvensis and its microbial symbiont community and between these organisms and their environment. Specifically, we used metaproteomics and metabolomics. We also used enzyme assays and in situ analyses of potential energy sources. Like the great majority of symbiotic microbes, the O. algarvensis symbionts have defied cultivation attempts, making cultivation-independent techniques like those used here essential for their analysis. While metagenomic analyses provide evidence for the metabolic potential of a microbial community, metaproteomic and metabolomic analyses can reveal the metabolic and physiological processes that actually are used by the community members. The microbiome of the worm O. algarvensis is highly specific and consists of five bacterial symbionts. Two of these symbionts are gammaproteobacterial sulfur oxidizers, two are deltaproteobacterial sulfate reducers, and the fifth is a spirochete ( 2 ). Previous studies, including metagenomic analyses of the bacterial symbionts, revealed how the worms can thrive in sulfide-poor coastal sediments of the Mediterranean ( 3 , 4 ). The sulfate-reducing δ-symbionts provide the sulfur-oxidizing γ-symbionts with reduced sulfur compounds as an internal energy source for the autotrophic fixation of CO 2 . However, the external sources of energy for the symbiosis that enable net growth and reproduction have remained unclear. Low nutrient availability is one of the major constraints for life on Earth, and organisms have evolved numerous strategies for overcoming this challenge. Symbiotic associations have been remarkably successful in enabling organisms to live in nutrient-poor environments. Particularly striking are the associations between chemosynthetic bacteria and marine animals, because the symbionts allow their hosts to thrive on inorganic energy and carbon sources such as sulfide and CO 2 , thus enabling them to flourish in habitats where they otherwise could not live, such as the deep sea or nutrient-limited shallow-water sediments ( 1 ). In this study, we reveal the intricate network of metabolic interactions in the gutless marine worm Olavius algarvensis and its chemosynthetic microbial community that could explain how this symbiosis thrives in its oligotrophic habitat. We propose previously undescribed pathways for coping with energy and nutrient limitations and show that some of these pathways may be widespread in both free-living and symbiotic bacteria ( Fig. P1 ).
Type of Medium:
Online Resource
ISSN:
0027-8424
,
1091-6490
DOI:
10.1073/pnas.1121198109
Language:
English
Publisher:
Proceedings of the National Academy of Sciences
Publication Date:
2012
detail.hit.zdb_id:
209104-5
detail.hit.zdb_id:
1461794-8
SSG:
11
SSG:
12
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