Dataset Information

Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress.

ABSTRACT: Large-scale mortality of marine invertebrates is a major global concern for ocean ecosystems and many sessile, reef-building animals, such as sponges and corals, are experiencing significant declines through temperature-induced disease and bleaching. The health and survival of marine invertebrates is often dependent on intimate symbiotic associations with complex microbial communities, yet we have a very limited understanding of the detailed biology and ecology of both the host and the symbiont community in response to environmental stressors, such as elevated seawater temperatures. Here, we use the ecologically important sponge Rhopaloeides odorabile as a model to explore the changes in symbiosis during the development of temperature-induced necrosis. Expression profiling of the sponge host was examined in conjunction with the phylogenetic and functional structure and the expression profile of the symbiont community. Elevated temperature causes an immediate stress response in both the host and symbiont community, including reduced expression of functions that mediate their partnership. Disruption to nutritional interdependence and molecular interactions during early heat stress further destabilizes the holobiont, ultimately leading to the loss of archetypal sponge symbionts and the introduction of new microorganisms that have functional and expression profiles consistent with a scavenging lifestyle, a lack virulence functions and a high growth rate. Previous models have postulated various mechanisms of mortality and disease in marine invertebrates. Our study suggests that interruption of symbiotic interactions is a major determinant for mortality in marine sessile invertebrates. High symbiont specialization and low functional redundancy, thus make these holobionts extremely vulnerable to environmental perturbations, including climate change.

SUBMITTER: Fan L

PROVIDER: S-EPMC3635241 | biostudies-literature | 2013 May

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress.

Fan Lu L Liu Michael M Simister Rachel R Webster Nicole S NS Thomas Torsten T

The ISME journal 20130103 5

Large-scale mortality of marine invertebrates is a major global concern for ocean ecosystems and many sessile, reef-building animals, such as sponges and corals, are experiencing significant declines through temperature-induced disease and bleaching. The health and survival of marine invertebrates is often dependent on intimate symbiotic associations with complex microbial communities, yet we have a very limited understanding of the detailed biology and ecology of both the host and the symbiont ...[more]

PMID: 23283017

Similar Datasets

Project description:Abstract Catch-and-release fishing is an important component of ecotourism industries and scientific research worldwide, but its total impact on animal physiology, health and survival is understudied for many species of fishes, particularly sharks. We combined biologging and blood chemistry to explore how this fisheries interaction influenced the physiology of two widely distributed, highly migratory shark species: the blue shark (Prionace glauca) and the tiger shark (Galeocerdo cuvier). Nineteen sharks were caught by drum line or rod-and-reel angling; subcutaneous body temperature measurements were taken immediately upon capture, with six individuals also providing subsequent subcutaneous body temperature measurements via biologging as they swam freely for several hours post-release. We found that short-term capture caused shark body temperature to increase significantly and rapidly, with increases of 0.6°C–2.7°C for blue sharks (mean, 1.2 ± 0.6°C) and 0.5°C–0.9°C for tiger sharks (mean, 0.7 ± 0.2°C) and with capture-induced heating rates of blue sharks averaging 0.3°C min−1 but as high as 0.8°C min−1. Blue shark body temperature was even higher deeper into the white muscle. These heating rates were three to eight times faster than maximum rates encountered by our biologging sharks swimming through thermally stratified waters and faster than most acute heating experiments conducted with ectotherms in laboratory experiments. Biologging data showed that body temperatures underwent gradual decline after release, returning to match water temperatures 10–40 mins post-release. Blood biochemistry showed variable lactate/glucose levels following capture; however, these concentrations were not correlated with the magnitude of body temperature increase, nor with body size or hooking time. These perturbations of the natural state could have immediate and longer-term effects on the welfare and ecology of sharks caught in catch-and-release fisheries and we encourage further study of the broader implications of this reported phenomenon.

Project description:Temperature exerts a first-order control on microbial populations, which constantly adjust the fluidity and permeability of their cell membrane lipids to minimize loss of energy by ion diffusion across the membrane. Analytical advances in liquid chromatography coupled to mass spectrometry have allowed the detection of a stunning diversity of bacterial and archaeal lipids in extreme environments such as hot springs, hydrothermal vents and deep subsurface marine sediments. Here, we investigated a thermal gradient from 18 to 101°C across a marine sediment field and tested the hypothesis that cell membrane lipids provide a major biochemical basis for the bioenergetics of archaea and bacteria under heat stress. This paper features a detailed lipidomics approach with the focus on membrane lipid structure-function. Membrane lipids analyzed here include polar lipids of bacteria and polar and core lipids of archaea. Reflecting the low permeability of their ether-linked isoprenoids, we found that archaeal polar lipids generally dominate over bacterial lipids in deep layers of the sediments influenced by hydrothermal fluids. A close examination of archaeal and bacterial lipids revealed a membrane quandary: not only low permeability, but also increased fluidity of membranes are required as a unified property of microbial membranes for energy conservation under heat stress. For instance, bacterial fatty acids were composed of longer chain lengths in concert with higher degree of unsaturation while archaea modified their tetraethers by incorporation of additional methyl groups at elevated sediment temperatures. It is possible that these configurations toward a more fluidized membrane at elevated temperatures are counterbalanced by the high abundance of archaeal glycolipids and bacterial sphingolipids, which could reduce membrane permeability through strong intermolecular hydrogen bonding. Our results provide a new angle for interpreting membrane lipid structure-function enabling archaea and bacteria to survive and grow in hydrothermal systems.

Dataset Information

Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress.

Publications

Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets