Characterization of the microbiome and bioluminescent symbionts across life stages of Ceratioid Anglerfishes of the Gulf of Mexico

Freed, Lindsay L; Easson, Cole G.; Baker, L.; Fenolio, Danté B.; Sutton, Tracey; Khan, Yasmin; Blackwelder, Patricia; Hendry, Tory A.; Lopez, Jose V.

doi:10.1093/femsec/fiz146

Cited by 20 publications

(29 citation statements)

References 50 publications

(75 reference statements)

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“…Enterovibrio luxaltus” and “ Ca. Enterovibrio escacola” have been found in water samples taken from the same locations sampled here ( 77 ), consistent with environmental persistence and possible environmental acquisition of symbionts.…”

Section: Resultssupporting

confidence: 80%

Ongoing Transposon-Mediated Genome Reduction in the Luminous Bacterial Symbionts of Deep-Sea Ceratioid Anglerfishes

Hendry

Freed

Fader

et al. 2018

mBio

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Diverse marine fish and squid form symbiotic associations with extracellular bioluminescent bacteria. These symbionts are typically free-living bacteria with large genomes, but one known lineage of symbionts has undergone genomic reduction and evolution of host dependence. It is not known why distinct evolutionary trajectories have occurred among different luminous symbionts, and not all known lineages previously had genome sequences available. In order to better understand patterns of evolution across diverse bioluminescent symbionts, we de novo sequenced the genomes of bacteria from a poorly studied interaction, the extracellular symbionts from the “lures” of deep-sea ceratioid anglerfishes. Deep-sea anglerfish symbiont genomes are reduced in size by about 50% compared to free-living relatives. They show a striking convergence of genome reduction and loss of metabolic capabilities with a distinct lineage of obligately host-dependent luminous symbionts. These losses include reductions in amino acid synthesis pathways and abilities to utilize diverse sugars. However, the symbiont genomes have retained a number of categories of genes predicted to be useful only outside the host, such as those involved in chemotaxis and motility, suggesting that they may persist in the environment. These genomes contain very high numbers of pseudogenes and show massive expansions of transposable elements, with transposases accounting for 28 and 31% of coding sequences in the symbiont genomes. Transposon expansions appear to have occurred at different times in each symbiont lineage, indicating either independent evolutions of reduction or symbiont replacement. These results suggest ongoing genomic reduction in extracellular luminous symbionts that is facilitated by transposon proliferations.

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Section: Resultssupporting

confidence: 80%

Ongoing Transposon-Mediated Genome Reduction in the Luminous Bacterial Symbionts of Deep-Sea Ceratioid Anglerfishes

Hendry

Freed

Fader

et al. 2018

mBio

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“…First, vertical samplings in the water column were performed using sterile-bag samplers (Ruby et al, 1980), or later using Niskin bottles (mounted on rosette profilers, Fig. 1c) (Al Ali et al, 2010;Gentile et al, 2009;Martini et al, 2016;Yetinson and Shilo, 1979). This approach is commonly set up in oceanography but relies on relatively small volumes of water (up to 20 L).…”

Section: Previous Sampling Methods To Describe Diversity and Abundancmentioning

confidence: 99%

“…Seasonal variations have been identified, in both abundance and predominant species (O'Brien and Sizemore, 1979;Ruby and Nealson, 1978;Yetinson and Shilo, 1979). A wide variability has been observed in species repartition over depth and between geographic areas (DeLuca, 2006;Gentile et al, 2009;Nealson and Hastings, 1979;Ramaiah and Chandramohan, 1992;Ruby et al, 1980). Horizontal, vertical and seasonal variations were presumed to reflect physiological preferences most of the time, and particularly temperature or salinity sensitivity (Orndorff and Colwell, 1980;Ramesh et al, 1990;Ruby and Nealson, 1978;Shilo and Yetinson, 1979;Yetinson and Shilo, 1979).…”

Section: Bioluminescent Bacteria In the Water Columnmentioning

confidence: 99%

Reviews and syntheses: Bacterial bioluminescence – ecology and impact in the biological carbon pump

et al. 2020

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Abstract. Around 30 species of marine bacteria can emit light, a critical characteristic in the oceanic environment is mostly deprived of sunlight. In this article, we first review current knowledge on bioluminescent bacteria symbiosis in light organs. Then, focusing on gut-associated bacteria, we highlight that recent works, based on omics methods, confirm previous claims about the prominence of bioluminescent bacterial species in fish guts. Such host–symbiont relationships are relatively well-established and represent important knowledge in the bioluminescence field. However, the consequences of bioluminescent bacteria continuously released from light organs and through the digestive tracts to the seawater have been barely taken into account at the ecological and biogeochemical level. For too long neglected, we propose considering the role of bioluminescent bacteria and reconsidering the biological carbon pump, taking into account the bioluminescence effect (“bioluminescence shunt hypothesis”). Indeed, it has been shown that marine snow and fecal pellets are often luminous due to microbial colonization, which makes them a visual target. These luminous particles seem preferentially consumed by organisms of higher trophic levels in comparison to nonluminous ones. As a consequence, the sinking rate of consumed particles could be either increased (due to repackaging) or reduced (due to sloppy feeding or coprophagy/coprorhexy), which can imply a major impact on global biological carbon fluxes. Finally, we propose a strategy, at a worldwide scale, relying on recently developed instrumentation and methodological tools to quantify the impact of bioluminescent bacteria in the biological carbon pump.

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“…The most common way to catch deep-sea animals is the deployment of trawls and more generally nets. They are well adapted to sample squid (Zamborsky and Nishiguchi, 2011) or fishes, like the anglerfish (Freed et al, 2019). One particularity of these methods is that the sampling covers a large section of the water column and pulled everything into one catch with a limited precision https://doi.org/10.5194/bg-2020-64 Preprint.…”

Section: Previous Sampling Methods To Describe Diversity and Abundancmentioning

confidence: 99%

Reviews and syntheses: Bacterial bioluminescence – ecology and impact in the biological carbon pump

Tanet¹,

Martini²,

Casalot³

et al. 2020

Preprint

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Abstract. Around thirty species of marine bacteria can emit light, a critical characteristic in the oceanic environment where the major part is deprived of sunlight. In this article, we first review current knowledge on bioluminescent bacteria symbiosis in light organs. Then, focusing on gut-associated bacteria, we highlight that recent works, based on omics methods, confirm previous claims about the prominence of bioluminescent bacterial species in fish guts. Such host-symbiont relationships are relatively well established and represent important knowledge in the bioluminescence field. However, the consequences of bioluminescent bacteria continuously released from light organ and through the digestive tracts to the seawater have been barely taken into account at the ecological and biogeochemical level. For too long neglected, we propose to consider the role of bioluminescent bacteria, and to reconsider the biological carbon pump taking into account the bioluminescence effect (bioluminescence shunt hypothesis). Indeed, it has been shown that marine snow and fecal pellets are often luminous due to microbial colonization, which makes them a visual target. These luminous particles seem preferentially consumed by organisms of higher trophic levels in comparison to non-luminous ones. As a consequence, the sinking rate of consumed particles could be either increased (due to repackaging) or reduced (due to sloppy feeding or coprophagy/coprorhexy) which can imply a major impact on global biological carbon fluxes. Finally, we propose a strategy, at a worldwide scale, relying on recently developed instrumentation and methodological tools to quantify the impact of bioluminescent bacteria in the biological carbon pump.

show abstract

Characterization of the microbiome and bioluminescent symbionts across life stages of Ceratioid Anglerfishes of the Gulf of Mexico

Cited by 20 publications

References 50 publications

Ongoing Transposon-Mediated Genome Reduction in the Luminous Bacterial Symbionts of Deep-Sea Ceratioid Anglerfishes

Ongoing Transposon-Mediated Genome Reduction in the Luminous Bacterial Symbionts of Deep-Sea Ceratioid Anglerfishes

Reviews and syntheses: Bacterial bioluminescence – ecology and impact in the biological carbon pump

Reviews and syntheses: Bacterial bioluminescence – ecology and impact in the biological carbon pump

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