Horizontal exchange of biological information and genesis of adaptive immune system

Article Citation: Petr Šíma and Vaclav Vetvicka. Horizontal exchange of biological information and genesis of adaptive immune system Journal of Research in Biology (2015) 5(1): 1619-1626 Jou

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Biology

Horizontal exchange of biological information and genesis

of adaptive immune system

Keywords: Evolution, Genes, Bacteria, Vertebrates

ABSTRACT:

Multicellular organisms have never evolved alone. Coevolution has been accomplished by means of horizontal information transition. A wide row of hierarchized interspecies interactions simultaneously transmitting biological information had evolved in the past. In the present review, we summarize the current hypothesis about possible horizontal exchange of biological information and genesis of adaptive immune system.

001-004 | JRB | 2015 | Vol 5 | No 1

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Authors:

Petr Šíma1 and Vaclav

Vetvicka2

Institution:

1.University of Louisville,

Department of Pathology,

Louisville, KY 40202, USA

2.Department of

Immunology and

Gnotobiology,

Institute of Microbiology,

Czech Academy of Sciences,

Vídeňská 1083, 142 20

Prague 4, The Czech

Republic

Corresponding author:

Vaclav Vetvicka

Web Address: http://jresearchbiology.com/

documents/RA0481.pdf

Dates: Received: 16 Sep 2014 Accepted: 19 Dec 2014 Published: 29 Jan 2015

Journal of Research in Biology

An International Scientific Research Journal

REVIEW

ISSN No: Print: 2231 –6280; Online: 2231- 6299

Horizontal exchange of biological information has a

substantial role in evolution

The first experimental evidence of the ability of

microorganisms to incorporate the foreign genetic

material into their genomes was referred in 1944 (Avery

et al., 1944). However, the idea of symbiosis of two or

more unrelated organisms, even pro- and eukaryotic, and

consequent exchange of their genetic material through

horizontal pathway, is much older. In 1867, Schwendener

was the first to consider the role of intrinsic coexistence of

two unrelated organisms in evolution. In 1879, De Bary

introduced the concept of symbiosis, which was further

completed by Merezhkowsky into the Theory of

symbiogenesis in 1920. Then, since the end of the 20th

century, owing to the comparative work of Margulis

(1993), it has been clear that the genes of mitochondria,

chloroplasts, and other organelles could be found

incorporated in the genome within the nucleus of their

eukaryotic cells.

Multicellular organisms have never evolved

alone, as evolution does not know a splendid isolation

from other living beings. Not evolution, but coevolution

formatted all organisms since the dawn of life.

Coevolution has been accomplished by means of

horizontal information transition. Acquisition of

horizontally transmitted genes explains the comments

written as early as 1970 (Anderson, 1970). This could be

the answer to Syvanen´s query “Why is molecular biology

so unified?” (Syvanen, 1994).

Defense of self vs. biological information exchange

The evolution of living organisms was

principally the hierarchized mutual coevolution of units,

thermodynamically open systems (Bertalanffy, 1950), so

called the CITROENS (Complex Information

Transforming, Reproducing Objects that Evolved by

Natural Selection), cooperating or competing with each

other for space, nutrition, and survival (Orgel, 1973).

Their life and adaptive radiation were constricted by the

horizontal exchange of biological information, and

simultaneously, by the defense of their internal integrity.

Pathways of biological information exchange

A wide row of hierarchized interspecies

interactions simultaneously transmitting biological

information had evolved in the past, which by means of

various molecules as information vectors and molecular

mechanisms in the role of receivers allowed

communication among non-related micro- and

macroorganisms (Table 1).

Šíma and Vetvicka, 2015

1620 Journal of Research in Biology (2015) 5(1): 1619-1626

*) relations without definition of differences between parasitism and profit

Interrelationship Mutual attitudes Vectors

Neutralism without mutual influence none

Protocooperation

relatively free, independent recipro-

cal profit

Attractants, allomones, kairomones, sinomones

Mutualism fully dependent reciprocal profit Attractants, allomones, kairomones, sinomones

Commensalism

relatively free profit for only one Attractants, pheromones, kairomones

Amensalism

Antibiosis

Allelopathy

negative influence annihilation of an

organism defense to competition

Inhibitors, antibiotics, deterrents, phytoncides, repellents

toxins

Competition mutual negative influence Inhibitors, antibiotics, deterrents, phytoncides, repellents

toxins

Parasitism attack toward an organism,

pathogenesis, gradual virulence Inhibitors, antibiotics, deterrents, phytoncides, repellents

Toxins, pathogenicity islands

Table 1. Interspecific relations and interactions among organisms (The symbiosis sensu De Bary (1869))*

At least two pathways of biological information

transfer could be regarded as fundamental: 1) the

indirect pathway represents a number of factors and

signal molecules of various chemical compositions,

which are released into the environment (Table 1 and 2)

the direct instructive pathway of biological information

transfer is represented by gene transmission, which is

mediated by an amalgamation of entire genomes of two

or more organisms, insertion of smaller genome regions

like single genes, and parts of genes (nucleotides). In this

case, the vectors represent mobile elements such as

viruses (bacteriophages), conjugative plasmids, free

nucleic acids (insertion elements, gene cassettes),

transposons, genomic islands, and possibly even prions

(Lee, 1996; Hacker and Carniel, 2001; Schmidt and

Hensel, 2004; Prusiner, 1994; Silvestri and Baldassarre,

2000).

Genomes are not protected by an immune system

It is not easy for a microbe, virus, or multicellular

parasite to enter into the internal milieu of a multicellular

eukaryotic organism. The mucus and cell membranes of

the external and internal epithelia are effective barriers

against the foreign invaders. In cases where these borders

have been damaged, or invading parasites developed

mechanisms to penetrate, a machinery of defense is

prepared to their neutralization and annihilation.

Immunocompetent cells producing a row of defense

molecules, including antibodies from immunoglobulin

superfamily, destroy the entire alien from outside.

Generally, there are three groups of enteric

bacterial pathogens categorized on the basis of the

mechanisms by which they cause disease. The bacteria of

the first group, exemplified by Vibrio cholerae and

Escherichia coli, could be characterized by mucosal

adherence and production of enterotoxins, which cause

diarrhea (Levine et al., 1983).

The bacteria of the second group (such as

Shigella) penetrate and proliferate within the intestinal

epithelia, which causes cell death. In some instances, they

discharge enterotoxins increasing lesions (Butzler and

Skirrow 1979; Levine et al., 1983).

Salmonella and Yersinia represent the third

group. These bacteria are able to translocate into intestinal

mucosa, and proliferate in the lamina propria and

mesenteric lymph nodes. Translocation of these bacteria,

particularly S. typhi and S. paratyphi A and B could be

followed by systemic bacteremia (Levine et al., 1983;

Beltran et al., 1988).

From the point of evolutionary view, when these

(and other) bacterial species capable of intracellular life

overcome the host immunity, they could represent

potential vectors or direct donors of genes like

Pathogenicity Islands (PAI), the groups of virulence genes

on bacterial chromosome that could transfer new

biological information into the eukaryotic genome. The

PAI, the term introduced in 1990 by Hacker, may

represent mobile distinct molecular elements that take

advantage of phage integration mechanisms. A question

remains - represent bacteria like Salmonella, Francisella,

and similar intracellular microbes bearing PAI or other

mobile elements, the contemporary evolutionary vectors

of new biological information? Could the infections

caused by these microorganisms in the instance that the

victims survive have evolutionary consequences?

Advent of jaw vertebrates

“One of the great events of revolutions in the

history of vertebrates was the appearance of jaws. The

importance of this evolutionary development can be

hardly overestimated, for it opened new lines of

adaptation and new possibilities for evolutionary

advancement to the vertebrates that expanded

immeasurably the potentialities of these animals. The

appearance of the jaws in vertebrates was brought about

by a transformation of anatomical elements that originally

had performed a function quite different from the function

of food gathering” (Colbert, 1980).

Similarly, the same evolutionary importance

could be attributed to the emergence of the adaptive

Journal of Research in Biology (2015) 5(1): 1619-1626 1621


immune system. System in which not only ancient cells

(like wandering and sessile macrophages), but also the

novelty specific only for deuterostomes, have started new

collaboration and cooperation utilizing and synthesizing

new regulative and defense molecules in newly fabricated

structures, tissues and organs (Table 2).

RAG time and emergence of the adaptive

immune system

Some 500 million years ago, the predecessors of

gnathostomes, the placoderms, emerged in primordial seas

(Flajnik and Masahara, 2010). Possibly in these

forerunners, the genomes of their immunocompetent cells

were waiting for acceptance of new biological information

enabling them by means of highly sophisticated

mechanism of molecular recombination to transform

immunoglobulin superfamily molecules into effective

defense vectors, the T and B receptors, antibodies, MHC,

and other molecules needed for functions of the adaptive

immune system.

Three events influenced the emergence of

adaptive immunity: evolution of gnathostomean basic

body pattern inclusive jaws, differentiation of new

immunocompetent structures inclusive lymphoid tissue

(particularly GALT), and acceptance of mobile

transposons of bacterial origin, the RAGs (Recombination

Activation Genes) allowing V(D)J recombination of

molecules of immunoglobulin superfamily (Sakano et al.,

1979; Agrawal et al., 1998) (Table 3).

Why RAGs transposed just into lymphoid cells?

The capability of translocation of intestinal

bacteria throughout the mucous lining and across

epithelia, and to penetrate into and survive within the

certain developmental stages of ancestral rapidly

renewing cell populations like lymphoid cell lineage,

could represent mechanisms of a new genetic information

transfer in the form of gene cassettes like RAG

transposons (Agrawal et al., 1998;Hiom et al., 1998;

Hansen and McBlane, 2000). On the other hand, the same

is true about the disability of primitive

immunorecognition of their hosts and a slightly effective

immune response to destroy them.

It has been generally accepted that lymphoid

cells in a role of intraepithelial immunocompetent cells in

all walls of the body make up at least a half of all the

lymphocytes the mammalian immune system possesses.

They are loners – slowly wandering free cells among the

epithelial cells. Evolutionary pressures like the threat of

decay of integrity of organisms caused by pathogens or

parasites and to counter the effects of somatic potential

carcinogenic mutations may be sufficient stimuli to



Taxon Cells Organs Molecules

Echinoderms lymphoid-like axial organ Ig

Protochordates lymphoid-like - Ig

Chordates lymphoid-like stolon -

Agnathans lymphoid typhlosole Ig

Gene cassettes incorporation into lymphoid cell lineage

Gnathostomes lymphocytes thymus RAG, TCR, BCR etc.

GALT

bursa Fabricii-like

spleen

lymph nodes

Table 2. Evolutionary consequences of gnathostomean basic body plan. Morphofunctional

prerequisites for adaptive immunity

develop rapidly renewing and specialized cell lineage that

could neutralize these threats (Millar and Ratcliffe, 1989).

The first lymphoid-like cell populations endowed

with the primitive T and B diversity were documented in

the axial organ of deuterostomian echinoderms, which is,

moreover, supposed as phylogenetic homolog of the

vertebrate spleen (Leclerc et al., 1993).

Urochordates contain several morphologically

distinct free cell types, but from the point of view of their

morphology and immune functions, the most important

cell type is considered to be the lymphocyte-like cell,

known also by name, the lymphocyte. The biological

characteristics of these cells include the participation in

encapsulation, allograft rejection, cytotoxicity,

proliferative response and immune memory (Sawada et

al., 1993).

In cyclostomes, the lymphohemopoietic cell

aggregations accompanying the veins in the intestine

submucosa are considered as an early form of GALT. In

these animals, which lack true thymus and spleen, these

aggregations form about one-tenth of the gut wall volume

(Grozdinski, 1926, Tanaka et al., 1981). In the larval stage

of the ammocoete, the main lymphohemopoietic organ

most often homologized to vertebrate spleen or bone

marrow is a longitudinal infolding along the anterior

intestine, the typhlosole (Šíma and Slípka, 1995) (Table

2).

In elasmobranches, the first living gnathostomean

vertebrates, the Leydig organ represents the important

lymphomyeloid structure associated to the anterior gut

(Zapata 1981; Zapata and Cooper 1990).

In osteichthyan fish, the presence of gut

lymphoid tissue has been documented, although they do

not possess structures like follicles resembling Peyer´s

patches (Hart et al., 1988).

In amphibians, the first vertebrates, which have

adapted to terrestrial life, the intraepithelial lymphoid

cells within the gut lamina propria and encapsulated

lymphoid structures in the oesophagus have been

described (Ardavin et al., 1982; Wong, 1972).

Intraintestinal epithelium of reptiles contains

numerous intraepithelial lymphoid cells including

plasmacytes. Lymphoid cell aggregates in the gut

submucosa resemble Peyer´s patches precursors in

mammals. Similar accumulations were found on body

locations of avian bursa of Fabricius or mammalian

appendix (Solas and Zapata, 1980, Zapata and Solas,

1979).

Birds possess the well-developed GALT exerting

many similarities to that of mammals: Peyer´s patches

(Basslinger, 1858; Befus et al., 1980), cecal lymphoid

nodules and tonsils (del Cacho et al., 1993; Glick et al.,

1981), and in addition, the cloacal diverticulum

specialized to B cell development and production, the

bursa of Fabricius (Glick, 1978; Jeurissen et al., 1989)

(Table 2).

What happened before the emergence of

gnathostomian vertebrates?

It may be hypothesized with a high probability

that the lymphoid cell lineage of predecessors of

gnathostomes was sufficiently plastic for acceptation of

RAG gene cassettes and for incorporation of them into

suitable loci of chromosomes. According to current



- Unrelated in sequence, tightly linked

- Cleavage pathway similar to steps involved in DNA transposition reactions

- Retroviral type of integration

- DNA breakage and rejoining by means of trans esterification of mobile elements

- RAG and HIV integrases use alcohol instead of water as the nucleophile in the DNA cleavage reaction

Table 3. Characters of Recombination Activation Genes (RAG1 and RAG2) suggesting horizontal transfer

knowledge, the sources of RAGs had to be some species

of bacteria that could enter into lymphoid cells, adapt to

intracellular life, and transport a part of their chromosome

into nuclear genome apparatus. These originally infectious

bacteria could be endowed by a low degree of virulence

and might be capable to co-exist within cells for many

millions of years in some form of symbiosis like

protocooperation, mutualism or commensalism (Table 1).

Several questions remain. One focuses on

contemporary intracellular parasites such as Salmonella,

Shigella, Francisella etc., serving as potential vectors of

new biological information. Can they be considered an

evolutionary novelty? Are extant birds and mammals

bearing intracellular parasites in their highly organized

GALT interconnected with gut epithelia the predecessors

of new species endowed with new evolutionary features

like the ancestors of gnathostomes?

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