Why does a true male, one in a thousand, walk lying down?

Hmm, before we get to today's protagonist

first, a warning for those afraid of bugs _(:з"∠)_

If you were asked what the most numerous group of organisms on Earth is, you'd probably guess some kind of single-celled microbe.

If we don't count single-celled organisms,the multicellular animals with the greatest number of individualswhich group would that be? Nematodes. You might not be able to come up with this answer, but this group has produced a laboratory animal that has won the Nobel Prize again and again--Caenorhabditis elegansCaenorhabditis elegans。

Hmm? What are nematodes? And howelegantare they? How could they also winthe Nobel Prize?

Caenorhabditis elegans under a microscope. Image: kdfj / wikimedia

They are everywhere

Caenorhabditis elegans belongs to the phylum Nematoda, which contains more than 25,000 species of invertebrates. In a suitable environment, tens of millions of nematodes may live in every square meter. Calculated by number of individuals, on Earth80%of animals are nematodes--if all the animals in the world lined up, between you and the next "non-nematode"there would be an average of four nematodes。

A root-knot nematode trying to burrow into a tomato root. Image: William Wergin & Richard Sayre / Wikimedia

This group of organisms, usually overlooked, is the most widely distributed group in Earth's biosphere; they can be found at the poles, in high mountains, deserts, and on the ocean floor. Nathan Cobb, a pioneer of American nematode taxonomy, once said that if all matter in the universe except nematodes instantly disappeared, then the nematodes floating in the void would be areplica of Earth's surface--mountains, rivers, lakes, seas, towns, villages, and even trees and animals could probably have their outlines restored through the specific species of nematodes distributed within them.

However, nematodes are not just the "strongest on the surface." In 2011, scientists discovered nematodes feeding onbacteriaon the surface of a gold mine several kilometers underground in South Africa. In addition, a considerable number of nematodes areparasitic, such as theroundworm。

The diversity of the phylum Nematoda, in which a is a roundworm and b is Caenorhabditis elegans. Image: Blumenthal & Davis / Nature Genetics (2004)

Compared with the noodle-like roundworm, which can reach 30 cm in body length, Caenorhabditis elegans is delicate and small, with mature individuals only 1 mm long, pointed at both head and tail, and with a freely bendable cylinder in the middle. Its genus name Caenorhabditis contains the root meaning "rod-like" (rhabditis), while the species name elegans means "beautiful, elegant." Look at Caenorhabditis elegansmoving like a sine wave, and you will probably understand how this completely transparent, colorless "little worm" got its name. Also, unlike the roundworm, Caenorhabditis elegans is anon-parasitic nematode。

The "elegant" way Caenorhabditis elegans moves forward. Image: Bob Goldstein / wikimedia

Nematodes just walk lying down

Though nematodes are small, they have all the "internal organs."As animals that, like humans, have three germ layers in development, the ectoderm of Caenorhabditis elegans develops into a "syncytium" formed by the fusion of multiple cells, and it is the collagen secreted by this layer that formsthe "skin" covering the whole body, an "exoskeleton" that can be shed and renewed as the worm grows. This is also one of the characteristics of the phylum Nematoda, indicating that they are closely related to the also-molting phylum Arthropoda.

The arrows show the "exoskeleton" formed by the fusion of different parts of the nematode body. Image: wormatlas.com

Below the cuticle are fourmuscle bandsrunning lengthwise through the body, formed from the mesoderm and controlled by a set of interconnected nerve cells. Because of the way the muscles contract, what you see in the gif is actually a "bending" in the dorsal-ventral direction, so a normal Caenorhabditis elegans alwayswalks lying on its side。

Immunofluorescence staining outlines the muscle bundles of Caenorhabditis elegans. Image: wormbook.org

Inside the muscles is a pseudocoelom filled with fluid, and further inside is astraight digestive tract--behind the mouth is the pharynx, attached to muscle cells and able to crush food, and further back is the intestine; before and after the intestine, a small ring of cells forms two "valves" that can open and close, equivalent to our human cardia (the entrance from the esophagus into the stomach) and anus. The long gonad lies right beside the digestive tract.

Only one in a thousand is a "true male"

From a human perspective, the reproductive mode of Caenorhabditis elegans is rather peculiar, divided into two sexes: "hermaphrodite" and "male." In a normally growing population,the vast majority of individuals are hermaphrodites: at the not fully mature stage of development, the hermaphrodite produces sperm and stores it in the gonad; when the individual matures, it produces eggs, which combine with the ready sperm to form fertilized eggs.

The internal structure of a hermaphrodite. Image: wormatlas.org

Strictly speaking, a hermaphrodite is a kind of female, with a genome that includes five pairs of autosomes and two X sex chromosomes. The sperm and egg cells produced each contain one set of five autosomes and one X chromosome, so after fertilization, the embryos produced are naturally mostly hermaphrodites (5*2+2X).

However, there is a very small probability that a fertilized egg randomly loses one X chromosome, and it will then develop into a male individual, trulya "true male" one in a thousand(5*2+X). Hermaphrodite self-fertilization can produce about 300 fertilized eggs, while after a male individual fertilizes a hermaphrodite, the number of offspring can exceed 1,000.

After encountering a hermaphrodite, the male makes "intimate contact" with it, using the fan-shaped structure at its tail to find the opening of the gonad and fertilize it. Image: Kbrugman / wikimedia

How the Nobel Prize triple kill was completed

The most important identity of Caenorhabditis elegans is as a scientific researchmodel organism. In the 1950s, when genetics research was beginning to flourish, South African biologist Sydney Brenner made great contributions to the development of molecular biology, but afterward he shifted his interest to the mechanisms of neural development in organisms. However, the human nervous system consists of 100 billion neurons, so how could it be studied? Brenner found the "highly skilled" Caenorhabditis elegans.

First, Caenorhabditis elegansis small, eats simply, grows quickly, and has strong vitality--after growing a layer of Escherichia coli on the agar plates commonly used in laboratories, nematodes can be placed on them, and the nematodes can happily eat and reproduce; at room temperature they can reproduce for one generation in three or four days, and their lifespan is about three weeks.The experimenters want a holiday?No problem.Just put the plates directly into a -80°C freezer and freeze them; after going out and having fun, come back and thaw them, and the nematodes will still be lively. Hermaphrodites that self-fertilize can conveniently be passaged, while the existence of males also facilitates crosses between different genotypes.

In the middle of the culture dish is an Escherichia coli colony, and the black ring around it is a soil sample containing Caenorhabditis elegans (A); nematodes that feed on bacteria are attracted by the food and burrow out of the soil, and these active nematode individuals are picked out for the next generation of reproduction (B). Image: Antoine Barrière & Marie-Anne Félix / wormbook.org

Second, the nematode'ssimple yet complete body structure is a very good starting point for research. In 1983, British scientist John Sulston studied the developmental process of Caenorhabditis elegans. In an era without advanced instruments, Sulston relied on observing the transparent worm body with the naked eye under an optical microscope and mapped the developmental atlas of all the nematode's cells--starting from the first division of the fertilized egg, every cell division and every cell's function and fate in the nematode are completely determined. This was the world's first cell lineage of a multicellular organism.

Using dots to represent nerve cell bodies and lines to represent dendrites and axons of nerve cells, scientists mapped the nematode's nerve cell atlas. Image: The OpenWorm

Today, almost all developmental biology textbooks mention that during development, the hermaphrodite nematode produces 1,090 cells, of which 131 initiate a normal apoptosis program after being produced and die, leaving only 959. In 2002, the Nobel Prize in Physiology or Medicine was awarded to three scientists--Brenner, Sulston, and Horvitz (Howard Robert Horvitz)--for their contributions tothe regulation of organ development and programmed cell death research. On the Nobel Prize list, the nematodescored first blood。

From left to right are Brenner, Horvitz, and Sulston; sadly, Sulston passed away in March 2018. Image: nobelprize.org

Only four years later, the Nobel Prize in Physiology or Medicine was awarded to Andrew Fire and Craig Mello for clarifyingthe RNA interference mechanism in nematodes--from a blank control group that did not match expected results, the two discovered that organisms can detect pathogenic double-stranded RNA and use it as a "guide" to attack the pathogen's genome. Now, the RNA interference mechanism has become a common tool in biological research. The nematode deservedly achieved a Nobel Prizedouble kill。

In the 2008 Nobel Prize in Chemistry, one of the three laureates, Martin Chalfie, usedgreen fluorescent proteinin nematode research. The nematode completed a Nobel Prizetriple kill。

Caenorhabditis elegans inserted with a gene encoding green fluorescent protein. Image: Dan Dickinson, Goldstein lab, UNC Chapel Hill

In fact, nematodes have even broader applications in biological research. In 1998, through a "preliminary experiment" of the Human Genome Project, Caenorhabditis elegans became the world'sfirst multicellular organism to have its whole genome sequenced. And as of 2012, the nematode neural network composed of 302 cell connections had also completed "connectome" mapping.

The elegant Caenorhabditis elegans will continue to reveal the wonders of life's mechanisms to humanity.

Life is full of mysteries, like another universe. The image shows Caenorhabditis elegans after fluorescent staining of the nucleus. Image: queensu.ca

This article is the 237th article of the 4th year of Species Calendar, from Species Calendar author @Lu Ping.

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