Unintelligent Design - A Heath-Robinson Solution To A Simple Problem

Convolutriloba longifissura.
Fluorescence imaging shows the algal cells in red, and the acoel cells in blue and green.

Dania Nanes Sarfati

Convolutriloba longifissura. The green body color of the adult comes from algal symbionts integrated in its skin. The red stripes in the middle of the body of this 3 millimeter long worm indicate mature oocytes.

Credit: Eric Rottinger/www.Kahikai.org
National Science Foundation - Media Gallery

The surprising relationship between marine worms and the algae that live inside them | Stanford Report

Creationists who like to cite complexity as evidence of intelligent design, either don't understand design or believe the designer is a bumbling idiot who never settles for a simple solution when a more complicated one is available, and never misses an opportunity to make a mountain out a molehill, as my old mother used to say if we turned a small problem into a big one.

That's of course, if you believe that creationist superstition of magic creation and not the scientifically proven, evolution, as an explanation for the form of living things.

Imagine you're a creator who is designing a simple marine flatworm and you decide that just what it needs is to be able to make food the way plants do, using the energy in sunlight to turn carbon dioxide into sugars. You previously designed some bacteria to perform this process, then, in an earlier invention, you put some of these bacteria in a single-celled plant and made algae. You could have given the single-celled plant the same enzymes and metabolic pathway you gave the bacteria but that was too simple, so you put the bacteria inside the plant cell as cell organelles called chloroplasts.

Tell me all about the marine flat worm Convolutriloba longifissura, please. Convolutriloba longifissura is a species of acoelomorph worm that inhabits marine environments. Here are some key details about this fascinating organism:

Taxonomy and Classification

• Kingdom: Animalia
• Phylum: Acoelomorpha
• Class: Acoela
• Order: Acoelida
• Family: Convolutidae
• Genus: Convolutriloba
• Species: Convolutriloba longifissura

Morphology and Anatomy

• Size and Shape: Convolutriloba longifissura are small, flattened worms. They are typically only a few millimeters in length.
• Body Structure: They lack a true gut and body cavity, characteristic of acoelomorphs. Instead, their digestive system consists of a simple gastrovascular cavity.
• Symbiotic Algae: These worms often contain symbiotic algae within their tissues, which provide them with nutrients through photosynthesis. This relationship is beneficial for both the worm and the algae.

Reproduction

• Asexual Reproduction: Convolutriloba longifissura is well known for its remarkable method of asexual reproduction, specifically through transverse fission. The worm can split itself into two or more parts, each of which regenerates into a complete organism. The name "longifissura" hints at this long splitting process.
• Regeneration: Post-fission, each segment is capable of regenerating the missing parts, making this species a subject of interest in the study of regenerative biology.

Habitat

• Marine Environment: These worms are found in marine environments, often associated with coral reefs and shallow coastal waters. They prefer habitats where they can benefit from their symbiotic algae.

Behavior

• Locomotion: Convolutriloba longifissura moves using cilia on its ventral surface, gliding smoothly over substrates in its habitat.
• Feeding: The diet consists mainly of small particles and microorganisms. Their symbiotic relationship with algae also plays a crucial role in their nutrition.

Ecological Role

• Symbiosis and Ecosystem Interaction: As part of the marine ecosystem, they play a role in nutrient cycling and serve as a food source for other marine animals. Their relationship with symbiotic algae also contributes to primary production in their habitats.

Research Significance

• Regeneration Studies: The ability of Convolutriloba longifissura to regenerate its body parts makes it an important model organism in scientific research, particularly in studies related to developmental biology and regenerative medicine.
• Evolutionary Insights: Studying this worm provides insights into the early evolution of bilaterian animals, given its position in the phylogenetic tree.

Conservation Status

• Population and Threats: There is limited information on the conservation status of Convolutriloba longifissura specifically. However, like many marine organisms, they could be affected by habitat degradation, pollution, and climate change.

Fun Fact

• Bioluminescence: Some species within the Convolutriloba genus are known for their bioluminescence, although it is not well-documented if Convolutriloba longifissura exhibits this trait.

In summary, Convolutriloba longifissura is a small but remarkable marine worm notable for its asexual reproduction through fission, its symbiotic relationship with algae, and its significance in scientific research on regeneration and evolutionary biology.

But what about these flatworms?

You now have three choices: you can give them the same enzymes and processes you gave the bacteria, but that was too simple for the algae, so why make it that easy for the flatworm? You could put the bacteria in the flat-worm cells like you did with the algae; but why do that when there is an even More complicated method? The third choice is to put the algae inside the flatworms and, as that's the most complicated way of doing it, why not go for that solution?

This is, of course, an example of the mutualist symbiotic association that is commonplace throughout nature and is a predictable result of 'selfish' genes forming alliances that are in the interest of both organisms (or in this case, three organisms, if you regard the algae as two organisms already in a symbiotic relationship)

But there is now another problem!

You have also designed a complicated way for these flatworms to reproduce. They split in two transversely, then the head end grown a new tail and the tail grows not one new head but two, then it splits lengthwise into two new worms!

So, the problem now is how to ensure the supply of algae is divided up and reproduces to give each of the three offspring enough manufactured sugar. Obviously, that needs to be coordinated with the flatworm's regeneration. It's no good growing into a bigger flatworm unless your symbiont algae replicate too, but why should they if they are autonomous cells simply living inside the worms?

So how, as creationism's intelligent [sic] designer, can you come up with a complicated solution to this problem of which William Heath-Robinson would be proud?

How it was actually done was the subject of a recent research paper published, open access, in Nature Communications by researchers led by Assistant Professor Bo Wang of Stanford University in conjunction with colleagues from San Francisco University who studied the acoel, Convolutriloba longifissura. Their research is the subject of a news release from Stanford University:

Regenerating worms have genetic control over their algal partners

Researchers at Stanford have found a genetic pathway that facilitates interspecies communication between a marine worm, acoel, and its symbiotic algae.

Many organisms are far more complex than just a single species. Humans, for example, are full of a variety of microbes. Some creatures have even more special connections, though. Acoels, unique marine worms that regenerate their bodies after injury, can form symbiotic relationships with photosynthetic algae that live inside them. These collections of symbiotic organisms are called a holobiont, and the ways that they “talk” to each other are something scientists are trying to understand – especially when the species in question are an animal and a solar-powered microbe.

Bo Wang, assistant professor of bioengineering in the Schools of Engineering and of Medicine at Stanford, has started to find some answers. His lab, in conjunction with the University of San Francisco, studies Convolutriloba longifissura, a species of acoel that hosts the symbiotic algae Tetraselmis. According to new research, published in Nature Communications, the researchers found that, when C. longifissura regenerates, a genetic factor that takes part in the acoel regeneration also controls how the algae inside of them reacts.

We don’t know yet how these species talk to each other or what the messengers are. But this shows their gene networks are connected.

Assistant Professor Bo Wang, co-corresponding author.
Department of Bioengineering
Stanford University, Stanford, CA, USA.

Splitting worms
Because holobiont is a relatively new concept, scientists still aren’t sure what the nature of some relationships are. The odd name “acoel” is Greek for “no cavity,” as the worms have no separation between their inner and outer organs (called a coelom). In these animals, all their organs share the same space. Some acoels also have symbiotic algae sharing the space of the animals' organs, and photosynthesizing inside the animals' body. This relationship provides a safe zone for the algae and extra energy from photosynthesis to the acoel.

There was no guarantee that there was communication because the algae are not within the acoel’s cells, they’re floating around them.

James Sikes, co-corresponding author
Department of Biology
University of San Francisco, San Francisco, CA, USA.

Sikes has been working with acoels for about 20 years, and their symbiotic relationship differentiates them from other animals that regenerate, like planarian flatworms and axolotls.

When these acoels reproduce asexually, they first bisect themselves. The head region grows a tail and becomes a new acoel. The tail, however, acts like the mythological Hydra and grows two new heads, which, then, split into two separate animals.

Animal regeneration requires communication across many different cell types, but in this case, it may also involve another organism entirely. Researchers were curious about how the algal colonies inside reacted to this process – in particular, whether they continued to photosynthesize as normal, and if not, what was controlling that? This was especially puzzling as the team found that photosynthesis wasn’t required for acoels to regenerate – they could do it in the dark. But there has to be conversation between the species for their long-term survival.

Convolutriloba longifissura by Deep Look, a series from KQED and PBS Digital Studios.

Testing if photosynthesis was affected was an adventure. None of us knew what we were doing. One of the most exciting things was that we could actually measure algal photosynthesis happening inside the animal.

Dania Nanes Sarfati, lead author
Department of Biology
Stanford University, Stanford, CA, USA.

In addition, through sequencing, the team was able to differentiate the genes of the two species and figure out which pathways were responding to injury. These measurements helped them realize that the algae inside were undergoing a major reconstruction of their photosynthetic machinery during the regeneration – but the process by which it was being controlled was shocking.

The role of runt
When the results came back, Wang said the unpredictable happened. During regeneration, both the acoel’s regrowth and the algal photosynthesis appeared to be controlled by a common transcription factor in acoels called runt.

In the early stage, right after injury, runt is activated, kicking off the regeneration process. Meanwhile, algal photosynthesis drops off, but there is an upregulation in algal genes associated with photosynthesis – likely to compensate for the loss in photosynthesis due to the split. However, when the researchers knocked down runt, it halted both regeneration and the algal responses.

What’s special about runt is that it’s highly conserved, meaning the same factor is responsible for regeneration in many different organisms, including non-symbiotic acoels. But now it’s clear that instead of just controlling the acoel’s regenerative process, it also controls the communication with another species.

How holobionts communicate
Understanding how partners in symbiotic relationships communicate at the molecular level opens up many new questions for this field of research.

Are there rules of symbiosis? Do they exist?. This research sparks these kinds of questions, which we can link to other organisms.,/P.

Nanes Sarfati.

Wang believes it introduces more ways of investigating how symbiotic species interact and couple with each other to form holobionts. Some of these interactions could be potentially driven by chemicals, proteins, or environmental factors. But more concerningly, these interactions are now becoming vulnerable points under the challenge of climate change, causing symbiotic partners to separate. Sikes highlighted that he, Wang, and Nanes Sarfati all began from the animal side of the symbiotic relationship but realized that algae respond to host injury as well, potentially sparking similar questions in other systems.

We often assume we know a lot, but we’re humbled when we look at different species. They can do things in completely unexpected ways, which highlights the need to study more organisms and is becoming possible with technology.

Bo Wang

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Additional Stanford co-authors include former graduate student Yuan Xue, PhD ’21; PhD student Eun Sun Song; Stephen Quake, the Lee Otterson Professor of Bioengineering in the Schools of Engineering and Medicine and professor of applied physics in the School of Humanities and Sciences; and Adrien Burlacot, assistant professor (by courtesy) of biology in the School of Humanities and Sciences.

Abstract
Animal regeneration involves coordinated responses across cell types throughout the animal body. In endosymbiotic animals, whether and how symbionts react to host injury and how cellular responses are integrated across species remain unexplored. Here, we study the acoel Convolutriloba longifissura, which hosts symbiotic Tetraselmis sp. green algae and can regenerate entire bodies from tissue fragments. We show that animal injury causes a decline in the photosynthetic efficiency of the symbiotic algae, alongside two distinct, sequential waves of transcriptional responses in acoel and algal cells. The initial algal response is characterized by the upregulation of a cohort of photosynthesis-related genes, though photosynthesis is not necessary for regeneration. A conserved animal transcription factor, runt, is induced after injury and required for acoel regeneration. Knockdown of Cl-runt dampens transcriptional responses in both species and further reduces algal photosynthetic efficiency post-injury. Our results suggest that the holobiont functions as an integrated unit of biological organization by coordinating molecular networks across species through the runt-dependent animal regeneration program.

Introduction
The concept that multicellular organisms can only exist in conjunction with their symbionts has profoundly transformed our understanding of a variety of biological processes. The term “holobiont” has been introduced to refer to the collection of a multicellular organism and its microbial symbionts. This term carries an important implication: the host and its symbionts must function together as an integrated unit of biological organization^1,2. Supporting this, studies on holobionts have revealed impacts of multispecies integration on physiological, behavioral, evolutionary, and developmental processes^3,4. There has been a particular focus on how symbionts influence host development, such as Vibrio fischeri guiding the formation of the squid’s light organ^5,6 and Blochmannia rewiring Hox genes during the embryonic development of Camponotini ants⁷. Conversely, the effects of the host on its symbionts during critical developmental processes, which could significantly affect the holobiont as a whole, is of equal importance but has been less explored. Tissue regeneration is one such critical event. Regeneration is widely observed in the animal kingdom, though varies greatly among species^8,9. Studies on animals, such as axolotl, zebrafish, planarian, and hydra, have demonstrated that regeneration involves intricate coordination across different cell types^10,11,12. Considering animals as holobionts adds an additional layer of complexity as the regeneration program needs to be coordinated across species^13,14. Understanding whether and how endosymbionts respond to the host regeneration and whether symbiont responses are modulated by the host regeneration program can unravel the mechanisms by which holobionts integrate molecular networks across species to operate as a single biological unit.

Progress in this respect has been bottlenecked by our limited capacity to measure the physiological states of symbionts. Here we overcome this challenge by studying animal-algal photosymbiosis, a common type of endosymbiotic relationship found in many regenerative animals, particularly in the groups of Porifera, Cnidaria, Acoela, and Mollusca¹⁵. In this relationship, the animal host benefits from the photosynthetic capabilities of algal partners, which fix carbon into organic compounds by converting solar energy to chemical energy through the photosynthetic electron transport chain¹⁵. Importantly, photosynthesis can serve as a gauge for algal physiology. In free living algae, photosynthesis is modulated by multiple abiotic factors including light¹⁶, nutrients¹⁷, temperature¹⁸, and the availability of inorganic carbon¹⁹. In photosymbiosis, hosts can regulate the photosynthetic output of their endosymbiotic algae by modulating the concentrations of inorganic carbon and nitrogen^20,21, adjusting the pH of the symbionts’ microenvironment^22,23, and changing light intensity²⁴. The study of regeneration in photosymbiotic animals, though rarely explored²⁵, presents a great opportunity to unravel the molecular integration between host and symbionts.

Specifically, we study the photosymbiotic acoel Convolutriloba longifissura, a marine worm that maintains an obligate symbiosis with Tetraselmis green algae²⁶. The algae reside between acoel cells, making this relationship an extracellular endosymbiosis²⁷. The acoels acquire their symbionts after hatching, and can transfer the algae to their clonal progeny through asexual fission^28,29. C. longifissura fissions every few days, generating new individuals through regeneration of its entire body from tissue fragments^28,30. In contrast to embryonic development³¹, regeneration proceeds in the presence of algal symbionts.

C. longifissura has been grossly understudied and the molecular tools available to investigate its biology are generally lacking. Therefore, we first assembled high-quality transcriptomes for both the acoel and the alga and developed a suite of tools to evaluate the host and endosymbionts’ responses during regeneration at the molecular and physiological levels. We found that, along with the expected acoel responses, the algae exhibited an abrupt decrease in photosynthetic efficiency, accompanied by large scale transcriptional changes including the upregulation of pathways related to photosynthesis, carbon concentrating mechanisms, and chlorophyll biosynthesis during early phases of regeneration. Notably, this contrasts the transcriptional changes induced by light stress in a similar timeframe, implicating that host injury triggers algal responses different from common stress responses. These early responses were followed by a second, synchronized wave of transcriptional changes at later stages of regeneration in both the acoel and the algae. Knockdown of a conserved injury-induced acoel transcription factor, Cl-runt^32,33, blocked acoel regeneration, attenuated both the early and late transcriptional changes, and further decreased the operating yield of photosystem II (PSII). As the function of Cl-runt during acoel regeneration appears to be conserved, our results suggest that the acoel’s early wound response contributes towards integrating the responses across species within this holobiont.

Fig. 1: Acoel regeneration involves both acoel and algal cells.

a Schematic of a simplified phylogeny showing the position of symbiotic acoels, which belong exclusively to the Convolutidae family. The position of the Xenacoelomorpha is still debated⁹² as a basal bilaterian or a sister group to Ambulacrarians (dotted line). b Photograph of the acoel C. longifissura. Numbers mark the pairs of white concrement granules and blue arrows point to the three tail lobes. c Differential interference contrast image showing the acoel cells (transparent and red cells) intermingled with green-brown algal cells (a few examples are highlighted by arrows). d Transverse section at the second concrement granule pair showing the distribution of algae (green) along the animal dorsal ventral axis (D-V), imaged through autofluorescence at 647 nm. e Algal cells are ubiquitously distributed across the host body, except the eye spots (arrowheads), which are devoid of algae. f Regeneration from posterior and anterior facing wounds. Top: posterior regeneration, with blue arrowheads indicating the regenerated tail lobes. Bottom: anterior regeneration with black arrows pointing at the blastema. Note the new tissue is devoid of algae until 4 dpa. g BrdU staining of posterior (top) and anterior (bottom) facing wound sites at 0 and 24 hpa. A buildup of BrdU+ cells is visible at the anterior wound at 24 hpa. h Fluorescence in situ hybridization (FISH) of the neuronal marker prohormone convertase 2 (Cl-pc2) and nuclei staining with DAPI at various time points post-amputation. The blastema formation is evident by the accumulation of cells at 2 dpa based on the DAPI staining. Neural ganglia are regenerated by 3 dpa. Numbers represent animals in which the neural structure is consistent with the figure out of the total number of animals examined. i Snapshots showing algal motions at the boundary of anterior blastema at 3 dpa. Highlighted in magenta is an example of an algal cell moving towards the regenerated tissue. Yellow: original position. Time stamp is shown as minutes:seconds. The corresponding video is available as Supplementary Movie 2. Experiments were repeated at least twice (c, d, g, h) or ten times (e, f). Schematics are created with BioRender.com.

Nanes Sarfati, D., Xue, Y., Song, E.S. et al. Coordinated wound responses in a regenerative animal-algal holobiont. Nat Commun 15, 4032 (2024). https://doi.org/10.1038/s41467-024-48366-2

Copyright: © 2024 The authors.
Published by Springer Nature Ltd. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)

Given a couple of minutes, I would think most people, even a creationist, could think up a simpler way to give a flat worm the ability to photosynthesise sugars, especially someone who has already designed a system for doing just that for a bacterium, but that apparently was beyond the wit of creationism’s putative designer in the case of this marine flatworm.

I wonder if even a creationist can work out why that might appear to be the case.

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