A Zeaxanthin-Producing Bacterium Isolated from the Algal Phycosphere Protects Coral Endosymbionts from Environmental Stress

Abstract

Reef-building corals form a complex consortium with photosynthetic algae in the family Symbiodiniaceae and bacteria, collectively termed the coral holobiont. These bacteria are hypothesized to be involved in the stress resistance of the coral holobiont, but their functional roles remain largely elusive. Here, we show that cultured Symbiodiniaceae algae isolated from the reef-building coral Galaxea fascicularis are associated with novel bacteria affiliated with the family Flavobacteriaceae. Antibiotic treatment eliminated the bacteria from cultured Symbiodiniaceae, resulting in a decreased maximum quantum yield of PSII (variable fluorescence divided by maximum fluorescence [Fv/Fm]) and an increased production of reactive oxygen species (ROS) under thermal and light stresses. We then isolated this bacterial strain, named GF1. GF1 inoculation in the antibiotic-treated Symbiodiniaceae cultures restored the Fv/Fm and reduced the ROS production. Furthermore, we found that GF1 produces the carotenoid zeaxanthin, which possesses potent antioxidant activity. Zeaxanthin supplementation to cultured Symbiodiniaceae ameliorated the Fv/Fm and ROS production, suggesting that GF1 mitigates thermal and light stresses in cultured Symbiodiniaceae via zeaxanthin production. These findings could advance our understanding of the roles of bacteria in Symbiodiniaceae and the coral holobiont, thereby contributing to the development of novel approaches toward coral protection through the use of symbiotic bacteria and their metabolites. IMPORTANCE Occupying less than 1% of the seas, coral reefs are estimated to harbor ∼25% of all marine species. However, the destruction of coral reefs has intensified in the face of global climate changes, such as rising seawater temperatures, which induce the overproduction of reactive oxygen species harmful to corals. Although reef-building corals form complex consortia with bacteria and photosynthetic endosymbiotic algae of the family Symbiodiniaceae, the functional roles of coral-associated bacteria remain largely elusive. By manipulating the Symbiodiniaceae bacterial community, we demonstrated that a bacterium that produces an antioxidant carotenoid could mitigate thermal and light stresses in cultured Symbiodiniaceae isolated from a reef-building coral. Therefore, this study illuminates the unexplored roles of coral-associated bacteria under stressful conditions.

Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs

“…Moreover, bacteria have been observed inside many types of algae [9][10][11][12][13], indicating the existence of intracellular interactions. Bacteria are known to provide their algal hosts with vitamin B12 [14][15][16][17], increased iron bioavailability [18], carotenoids [19], and growthpromoting hormones [20], though the array of functions is likely much greater.…”

Holobiont Nitrogen Control and its Potential for Eutrophication Resistance in an Obligate Photosymbiotic Jellyfish

“…This is an essential shortcoming as bacteria also directly interact with Symbiodiniaceae [82,86]. Further corroborating a functional importance of these associations, coral holobionts host conserved algal-bacterial partnerships [83] and bacteria derived carotenoids have been shown to protect the algal endosymbionts (and thereby the holobiont) from environmental stress [87].…”

Ameliorating process parameters for zeaxanthin yield in Arthrobacter gandavensis MTCC 25325

“…Elsewhere, Thawornwiriyanun et al (2012) recorded 30 °C as an ideal temperature for zeaxanthin production in Sphingomonas natoria. In a recent study, after 192 h of thermal stress at 31.6 °C, Muricauda lutaonensis (a Flavobacteriaceae bacteria) showed zeaxanthin yield of 8.04 × 10 −2 µg/mL when grown in association with a coral Galaxea fascicularis and an alga Symbiodiniaceae (Motone et al 2020). They have suggested that carotenogenesis in M. lutaonensis was governed by oxidative stress and also mentioned that zeaxanthin produced from this bacterium helps the alga and coral holobiont in mitigating environmental stress by reducing the production of reactive oxygen species (ROS).…”