Small Antarctic worms (zoom) rely on microbes to resist the chill of the frigid waters where they live.
Michael Tangherlini, Marco Lo Martire
Imagine you're a designer with all the power you need and all the solutions you've designed earlier at your fingertips and your task is to redesign some marine worms that you designer earlier and put into an arctic environment, perhaps not realising they wouldn't survive if they got frozen.
So, what you have to do is give these marine worms some way to prevent this happening and so mitigating your earlier blunder.
At your disposal is the method you gave to some marine bacteria, and even some fish known as icefish, when you made similar blunders years earlier - you gave them some genes for making antifreeze to stop the contents of their cells freezing and the ensuing ice crystals from destroying them.
Do you give these marine worms the same genes you gave the bacteria?
Not if you're creationism's putative intelligent [sic] designer, you don't. That would be far too simple.
What you do is modify the bacteria so they can live inside the worms, and you modify the worms so they don't treat the bacteria as parasites - modifications which take far more redesigning than simply giving the worms those genes for making antifreeze you gave the bacteria and icefish.
Creationists regard this ludicrous degree of over-complication to achieve a simple outcome to be evidence of a supreme intelligence - which probably tells us more about the intellectual abilities of creationists than they might want to show.
How this symbiotic association between bacteria and the polychaete worms was discovered is the subject of an open access paper in the journal Science by a team from several Italian marine institutions, led by Cinzia Corinaldesi of the Department of Materials, Environmental Sciences and Urban Planning, Polytechnic University of Marche, Ancona, Italy.
The team collected scoops of marine sediment in water in which the temperature was -1°C, i.e., 1 degree below freezing, so any creature living there would need some sort of anti-freeze protection. From the sediment, the team captures three species of polychaetes, Leitoscoloplos geminus, Aphelochaeta palmeri, which both live on dead and decaying matter in the marine sediment, and Aglaophamus trissophyllus which is a predator.
On analysist the worms were found to contain two enzyme proteins associated with the bacteria, Meiothermus silvanus and Anoxybacillus flavithermus, know to produce proline and glycol, both of which reduce the freezing point of water. However, they found that none of the proteins were produced directly by the polychaetes themselves.
DNA analysis showed that two genera of bacteria, which are known to produce cryoprotective proteins of the type that were found in the worms, were present withing the polychaetes, however, these bacteria are absent from the sediment in which the worms live.
The conclusion it then that the bacteria don't infect the worms from their environment but are passed down from one generation to the next in a symbiotic relationship in which the worms gain anti-freeze so they can live in an otherwise hostile environment, while the bacteria get protection and nutrients.
AbstractFrom an evolutionary point of view, these Heath Robinson solutions to simple problems are nothing new; in fact, they are to be expected of an unintelligent, utilitarian process operating without a plan or goal.
The microbiome plays a key role in the health of all metazoans. Whether and how the microbiome favors the adaptation processes of organisms to extreme conditions, such as those of Antarctica, which are incompatible with most metazoans, is still unknown. We investigated the microbiome of three endemic and widespread species of Antarctic polychaetes: Leitoscoloplos geminus, Aphelochaeta palmeri, and Aglaophamus trissophyllus. We report here that these invertebrates contain a stable bacterial core dominated by Meiothermus and Anoxybacillus, equipped with a versatile genetic makeup and a unique portfolio of proteins useful for coping with extremely cold conditions as revealed by pangenomic and metaproteomic analyses. The close phylosymbiosis between Meiothermus and Anoxybacillus and these Antarctic polychaetes indicates a connection with their hosts that started in the past to support holobiont adaptation to the Antarctic Ocean. The wide suite of bacterial cryoprotective proteins found in Antarctic polychaetes may be useful for the development of nature-based biotechnological applications.
INTRODUCTION
Multicellular organisms in the oceans live in close association with their microbiomes, which provide their hosts with key functions including nutrient supply, defense mechanisms, and even additional metabolic pathways, thus representing an integral component of the holobiont, able to influence host physiology and increase adaptation to environmental conditions (1–3). Microbiome-host interactions are far more widespread than previously thought and can notably influence the auto-ecology of marine organisms, playing a role in the whole ecosystem’s health (4–6).
The host-associated microbiota changes from species to species, also in relation to a variety of environmental (i.e., geographic location, seasonal variations, and nutrient availability) (7, 8) and biological factors (i.e., metabolic state, feeding strategy, and host phylogeny) (9, 10). However, the presence of a stable core (i.e., any set of microbial taxa characteristic of a specific host or environment) (11), reported for several holobionts, suggests that some microbes and related genomic or functional features are essential for the well-being of the host species (12, 13).
Some specific bacterial taxa, indeed, can be vertically transmitted and persist across life stages and generations, favoring mutual adaptation (2, 14). Mechanisms of transmission of microbiome components to their hosts may include horizontal acquisition, which is generally based on a selection of beneficial bacterial members from the environment anew by each host generation (15, 16).
Microbiomes could also have a role in the host-microbe adaptation to extreme environmental conditions and in evolutionary processes (2, 17). In this regard, information on marine host-microbiota phylosymbiosis as an eco-evolutionary pattern, where the ecological relatedness of host-associated microbial communities parallels the phylogeny of related host species (18), is contrasting. In some organisms, phylosymbiosis has been documented even to different extents in specific portions of their body (2, 19), whereas in others, it seems not to have a primary role, suggesting the lack of strong affinity between bacterial members and their specific host lineage (20). The processes driving microbial associations and influencing the adaptations of marine organisms to environmental conditions are still open questions (21). The investigation in extreme ecosystems can certainly contribute to explore the co-evolutionary processes and ecological interactions of the microbiota-host associations. One of the most isolated continents on Earth, Antarctica, can provide additional information into the adaptation of marine life to extreme conditions.
The geological isolation, along with the stability of extreme environmental conditions, for more than 34 million years has produced a range of unique adaptations to low temperatures with a highly diverse fauna composed of around 17,000 marine invertebrate species and with the highest proportions of endemic species of the world ocean (22, 23).
In polar ecosystems, marine poikilotherm metazoans (i.e., in which the internal temperature is in equilibrium with the environmental temperature) must adapt to extreme cold conditions using different biological and physiological mechanisms, such as the slowdown in embryonic development and growth rate and increase in oxygen consumption to maintain homeostasis, to prevent internal liquid freezing and to induce the antioxidant defense system (23).
Previous studies also hypothesized the presence of thermal hysteresis proteins in the haemolymph of ectothermic invertebrates, such as Antarctic nemerteans (24) and terrestrial invertebrates (25), but no general conclusions could be provided. At the same time, microbes own functional traits for adaptation to low temperatures (26, 27) and, when associated with Antarctic benthic invertebrates, play key roles in several metabolic processes (28). However, information on the mechanisms adopted by marine invertebrates to cope with extreme cold and freezing conditions is limited and controversial (23, 29), and the role of their microbiota in these mechanisms is even neglected.
In the present study, we investigated the microbiome of three dominant endemic species of Antarctic polychaetes (Leitoscoloplos geminus, Aphelochaeta palmeri, and Aglaophamus trissophyllus; Fig. 1) that play a key role in the benthic trophic webs (30, 31). The identity, origin, and proteome of the microbiota associated with these Antarctic invertebrates, as well as the factors influencing its structure, including phylosymbiosis, were investigated to provide insights into the role of the microbiome in marine invertebrate adaptation to the extreme conditions of Antarctic ecosystems.
Fig 1. Antarctic polychaetes investigated in the present study.
Pictures of polychaetes investigated: Leitoscoloplos geminus (A), Aphelochaeta palmeri (B), and Aglaophamus trissophyllus (C).
Fig. 6. Conceptual model illustrating the role of Meiothermus and Anoxybacillus in cryo-resistance of Antarctic polychaetes.
The conceptual model shows the phylosymbiosis relationships between Meiothermus and the three species of Antarctic polychaetes (the detritivorous Aphelochaeta palmeri and Leitoscoloplos geminus and the predator Aglaophamus trissophyllus) and between Anoxybacillus and the two detritivorous species. These bacteria are negligibly represented in the sediments, where other bacterial members thrive. The symbiosis between Meiothermus and/or Anoxybacillus has been perpetuated over time and allows the production of specific bacterial proteins such as DnaK, triosephosphate isomerase (TPI), and proline dehydrogenase (PRODH) (produced by Meiothermus) and AcrR, and NarL (produced by Anoxybacillus).
Emanuela Buschi et al. ,
Resistance to freezing conditions of endemic Antarctic polychaetes is enhanced by cryoprotective proteins produced by their microbiome. Sci. Adv. 10, eadk9117 (2024). DOI: 10.1126/sciadv.adk9117
Copyright: © 2024 The authors.
Published by American Association for the Advancement of Science. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
At some point in the distant past, the bacteria in the relationship evolved the means to manufacture antifreeze, which allowed them to move into sub-zero waters and survive. At a later stage, these bacteria became parasites on polychaete worms but parasites that enabled the worms to move into the sediment in Antarctic conditions where there were few competitors for the detritus on which they fed, so there was clear selection pressure to accommodate the bacteria and even give them food and shelter in return for the ability to survive in sub-zero conditions.
But rather than accept that obvious and easily understood chain of events, creationists would rather believe this is all the result of an incompetent and wasteful designer whose designs just happen to look like they were unintelligently designed by a process without a plan.
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